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Plants interact with each other via a multitude of processes among which belowground communication facilitated by specialized metabolites plays an important but overlooked role. Until now, the exact targets, modes of action, and resulting phenotypes that these metabolites induce in neighboring plants have remained largely unknown. Moreover, positive interactions driven by the release of root exudates are prevalent in both natural field conditions and controlled laboratory environments. In particular, intraspecific positive interactions suggest a genotypic recognition mechanism in addition to non-self perception in plant roots. This review concentrates on recent discoveries regarding how plants interact with one another through belowground signals in intra- and interspecific mixtures. Furthermore, we elaborate on how an enhanced understanding of these interactions can propel the field of agroecology forward.

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Plant volatiles play an important role in intra- and interspecific plant communication, inducing direct and indirect defenses against insect pests. However, it remains unknown whether volatile interactions between undamaged cultivars alter host plant volatile emissions and their perception by insect pests. Here, we tested the effects of exposure of a spring barley, Hordeum vulgare L., cultivar, Salome, to volatiles from other cultivars: Fairytale and Anakin. We found that exposing Salome to Fairytale induced a significantly higher emission of trans-ß-ocimene and two unidentified compounds compared when exposed to Anakin. Aphids were repelled at a higher concentration of trans-ß-ocimene. Salome exposure to Fairytale had significant repulsive effects on aphid olfactory preference, yet not when Salome was exposed to Anakin. We demonstrate that volatile interactions between specific undamaged plants can induce changes in volatile emission by receiver plants enhancing certain compounds, which can disrupt aphid olfactory preferences. Our results highlight the significant roles of volatiles in plant-plant interactions, affecting plant-insect interactions in suppressing insect pests. This has important implications for crop protection and sustainable agriculture.

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Plants emit volatiles as signals to trigger broad physiological responses, including airborne defense (AD). Gong et al. (Nature 2023; 622: 139-145) recently reported the genetic framework of how plants use AD to combat aphids and viruses. The study elucidates the mutualistic relationships between aphids and the viruses they transmit, revealing the broad biological and ecological significance of AD.

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Plants exposed to volatiles emitted from artificially damaged conspecific or heterospecific plants exhibit increased resistance to herbivorous insects. Here, we examined whether volatiles from artificially damaged weeds affect maize growth and reproduction. Seven days after germination, maize seedlings were exposed to volatiles emitted by artificially damaged mugwort (Artemisia indica var. maximowiczii) or tall goldenrod (Solidago altissima) plants either separately, or as a mixture of the two, for seven days. Unexposed seedlings were used as controls. Treated and control seedlings were cultivated in an experimental field without any insecticides applied. Plants exposed to either of the three volatile treatments sustained significantly less damage than controls. Additionally, seedlings exposed to either goldenrod or mixed volatiles produced more leaves and tillers than control plants. Furthermore, a significant increase in the number of ears was observed in plants exposed to the volatile mixture. In all treated plants, ear sugar content was significantly higher than that in the controls. Further, we cultivated seedlings that were either exposed to the volatile mixture or unexposed, under the conventional farming method using pesticides. Similar significant differences were observed for sugar content, number of tillers, leaves, damaged leaves, and ears. Laboratory experiments were conducted to further evaluate the mechanisms involved in the improved performance of volatile-treated plants. A significant reduction in the growth of common armyworm (Mythimna separata) larvae was observed when maize plants were exposed to the volatile mixture. This treatment did not affect the amount of jasmonic acid in the seedlings, whereas salicylic acid content increased upon exposure. The characteristic differences in chemical composition of mugwort and goldenrod volatiles were confirmed and, in turn, the volatile mixture differed significantly from the volatiles of either species.

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Plant-plant signalling via volatile organic compounds (VOCs) has been studied intensively, but its contingency on abiotic conditions (e.g., soil nutrients, drought, warming) is poorly understood. To address this gap, we carried out a greenhouse experiment testing whether soil nutrients influenced signalling between potato (Solanum tuberosum) plants in response to insect leaf herbivory by the generalist caterpillar Spodoptera exigua. We placed pairs of plants in plastic cages, where one plant acted as a VOC emitter and the other as a receiver. We factorially manipulated soil nutrients for both emitter and receiver plants, namely: unfertilized (baseline soil nutrients) vs. fertilized (augmented nutrients). Then, to test for signalling effects, half of the emitters within each fertilization level were damaged by S. exigua larvae and the other half remained undamaged. Three days after placing larvae, we collected VOCs from emitter plants to test for herbivory and fertilization effects on VOC emissions and placed S. exigua larvae on receivers to test for signalling effects on leaf consumption and larval mass gain as proxies of induced resistance. We found that herbivory increased total VOC emissions and altered VOC composition by emitter plants, but these effects were not contingent on fertilization. In addition, bioassay results showed that receivers exposed to VOCs from herbivore-damaged emitters had lower levels of herbivory compared to receivers exposed to undamaged emitters. However, and consistent with VOC results, fertilization did not influence herbivore-induced signalling effects on receiver resistance to herbivory. In sum, we found evidence of S. exigua-induced signalling effects on resistance to herbivory in potato plants but such effects were not affected by increased soil nutrients. These results call for further work testing signalling effects under broader range of nutrient concentration levels (including nutrient limitation), teasing apart the effects of specific nutrients, and incorporating other abiotic factors likely to interact or covary with soil nutrients.

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In pioneering studies on plant-aphid interactions, we have observed that Vicia faba plants infested by aphids can transmit signals via the rhizosphere that induce aboveground defence in intact, neighbouring plants. The aphid parasitoid Aphidius ervi is significantly attracted towards intact broad bean plants grown in a hydroponic solution previously harbouring Acyrtosiphon pisum-infested plants. To identify the rhizosphere signal(s) possibly mediating this belowground plant-plant communication, root exudates were collected using Solid-Phase Extraction (SPE) from 10-day old A. pisum-infested and un-infested Vicia faba plants hydroponically grown. To verify the ability of these root exudates to trigger defence mechanisms against the aphids we added them to V. fabae plants grown in hydroponic solution, and tested these plants in the wind-tunnel bioassay to assess their attractiveness towards the aphids' parasitoids A. ervi. We identified three small volatile lipophilic molecules as plant defence elicitors: 1-octen-3-ol, sulcatone and sulcatol, in SPE extracts of A. pisum-infested broad bean plants. In wind tunnel assays, we recorded a significant increase in the attractiveness towards A. ervi of V. faba plants grown in hydroponic solution treated with these compounds, compared to plants grown in hydroponic treated with ethanol (control). Both 1-octen-3-ol and sulcatol have asymmetrically substituted carbon atoms at positions 3 and 2, respectively. Hence, we tested both their enantiomers alone or in mixture. We highlighted a synergistic effect on the level of attractiveness towards the parasitoid when testing the three compounds together in respect to the response recorded against them singly tested. These behavioural responses were supported by the characterization of headspace volatiles released by tested plants. These results shed new light on the mechanisms underlying plant-plant communication belowground and prompt the use of bio-derived semiochemicals for a sustainable protection of agricultural crops.

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In addition to positive effects on plant growth and resilience, sound alerts plants of potential danger and aids in defense. Sound guides plants towards essential resources, like water, through phonotropic root growth. Sound also facilitates mutualistic interactions such as buzz pollination. Molecularly, sound induces Ca2+ signatures, K+ fluxes, and an increase in reactive oxygen species (ROS) levels in a mechanosensitive ion channel-dependent fashion. We review the two major open questions in the field of plant acoustics: (i) what is the ecological relevance of sound in plant life, and (ii) how is sound sensed and transduced to evoke a morphophysiological response? We highlight the clear need to combine the ecological and molecular perspectives for a more holistic approach to better understand plant behavior.

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It has been proposed that plant-plant signalling via herbivore-induced volatile organic compounds (VOCs) should be stronger between closely related than unrelated plants. However, empirical tests remain limited and few studies have provided detailed assessments of induced changes in VOCs emissions across plant genotypes to explain genetic relatedness effects. In this study, we tested whether airborne signalling in response to herbivory between Solanum tuberosum (potato) plants was contingent on plant genetic relatedness, and further investigated genotypic variation in VOCs potentially underlying signalling and its contingency on relatedness. We carried out a greenhouse experiment using 15 S. tuberosum varieties placing pairs of plants in plastic cages, i.e. an emitter and a receiver, where both plants were of the same genotype or different genotype thereby testing for self-recognition, an elemental form genetic relatedness effects. Then, for half of the cages within each level of relatedness the emitter plant was damaged by Spodoptera exigua larvae whereas for the other half the emitter was not damaged. Three days later, we placed S. exigua larvae on receivers to test for emitter VOC effects on leaf consumption and larval weight gain (i.e. induced resistance). In addition, we used a second group of plants subjected to the same induction treatment with the same S. tuberosum varieties to test for herbivore-induced changes in VOC emissions and variation in VOC emissions among these plant genotypes. We found that herbivory drove changes in VOC composition but not total emissions, and also observed quantitative and qualitative variation in constitutive and induced VOC emissions among varieties. Results from the bioassay showed that the amount of leaf area consumed and larval weight gain on receiver plants exposed to damaged emitters were significantly lower compared to mean values on receivers exposed to control emitters. However, and despite genotypic variation in induced VOCs, this signalling effect was not contingent on plant genetic relatedness. These findings provide evidence of VOCs-mediated signalling between S. tuberosum plants in response to S. exigua damage, but no evidence of self-recognition effects in signalling contingent on variation in VOC emissions among S. tuberosum varieties.

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It is firmly established that plants respond to biotic and abiotic stimuli by emitting volatile organic compounds (VOCs). These VOCs provide information on the physiological status of the emitter plant and are available for detection by the whole community. In the context of plant-plant interactions, research has focused mostly on the defence-related responses of receiver plants. However, responses may span hormone signalling and both primary and secondary metabolism, and ultimately affect plant fitness. Here we present a synthesis of plant-plant interactions, focusing on the effects of VOC exposure on receiver plants. An overview of the important chemical cues, the uptake and conversion of VOCs, and the adsorption of VOCs to plant surfaces is presented. This is followed by a review of the substantial VOC-induced changes to receiver plants affecting both primary and secondary metabolism and influencing plant growth and reproduction. Further research should consider whole-plant responses for the effective evaluation of the mechanisms and fitness consequences of exposure of the receiver plant to VOCs.

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In response to volatiles emitted from a plant infested by herbivorous arthropods, neighboring undamaged conspecific plants become better defended against herbivores; this is referred to as plant‒plant communication. Although plant‒plant communication occurs in a wide range of plant species, most studies have focused on herbaceous plants. Here, we investigated plant‒plant communication in beech trees in two experimental plantations in 2018 and one plantation in 2019. Approximately 20% of the leaves of a beech tree were clipped in half in the spring seasons of 2018 and 2019 (clipped tree). The damage levels to leaves in the surrounding undamaged beech trees were evaluated 90 days after the clipping (assay trees). In both years, the damage levels decreased with a reduction in the distance from the clipped tree. In 2019, we also recorded the damage levels of trees that were not exposed to volatiles (nonexposed trees) as control trees and found that those that were located <5 m away from clipped trees had significantly less leaf damage than nonexposed trees. By using a gas chromatograph-mass spectrometer, ten and eight volatile compounds were detected in the headspaces of clipped and unclipped leaves, respectively. Among them, the amount of (Z)-3-hexenyl acetate in clipped leaves was significantly higher than that in nonclipped leaves. Our result suggests that green leaf volatiles such as (Z)-3-hexenol and (Z)-3-hexenyl acetate and other volatile organic compounds emitted from clipped trees induced defenses in the neighboring trees within the 5 m radius. The effective distances of plant‒plant communication in trees were discussed from the viewpoint of the arthropod community structure in forest ecosystems.

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Volatile organic compounds (VOCs) from 'emitting' plants inform the 'receiving' (listening) plants of impending stresses or simply of their presence. However, the receptors that allow receivers to detect the volatile cue are elusive. Most likely, plants (as animals) have odorant-binding proteins (OBPs), and in fact, a few OBPs are known to bind 'stress-induced' plant VOCs. We investigated whether these and other putative OBPs may bind volatile constitutive and stress-induced isoprenoids, the most emitted plant VOCs, with well-established roles in plant communication and defense. Molecular docking simulation experiments suggest that structural features of a few plant proteins screened in databases could allow VOC binding. In particular, our results show that monoterpenes may bind the same plant proteins that were described to bind other stress-induced VOCs, while the constitutive hemiterpene isoprene is unlikely to bind any investigated putative OBP and may not have an info-chemical role. We conclude that, as for animal, there may be plant OBPs that bind multiple VOCs. Plant OBPs may play an important role in allowing plants to eavesdrop messages by neighboring plants, triggering defensive responses and communication with other organisms.

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Herbivore-induced plant volatiles play important ecological roles in defense against stresses. However, if and which volatile(s) are involved in the plant-plant communication in response to herbivorous insects in tea plants remains unknown. Here, plant-plant communication experiments confirm that volatiles emitted from insects-attacked tea plants can trigger plant resistance and reduce the risk of herbivore damage by inducing jasmonic acid (JA) accumulation in neighboring plants. The emission of six compounds was significantly induced by geometrid Ectropis obliqua, one of the most common pests of the tea plant in China. Among them, (E)-4,8-dimethyl-1,3,7-nonatriene (DMNT) could induce the accumulation of JA and thus promotes the resistance of neighboring intact plants to herbivorous insects. CsCYP82D47 was identified for the first time as a P450 enzyme, which catalyzes the final step in the biosynthesis of DMNT from (E)-nerolidol. Down-regulation of CsCYP82D47 in tea plants resulted in a reduced accumulation of DMNT and significantly reduced the release of DMNT in response to the feeding of herbivorous insects. The first evidence for plant-plant communication in response to herbivores in tea plants will help to understand how plants respond to volatile cues in response to herbivores and provide new insight into the role(s) of DMNT in tea plants.

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Damage-associated molecular patterns (DAMPs) are an ancient form of tissue-derived danger or alarm signals that initiate cellular signaling cascades, which often initiate defined defense responses. A DAMP can be any molecule that is usually not exposed to cells such as cell wall components, peptides, nucleic acid fragments, eATP and other compounds. DAMPs might be revealed upon tissue damage or during attack. Typically, DAMPs are derived from the injured organism. Almost all eukaryotes can generate and respond to DAMPs, including plants. Besides the molecules mentioned, certain volatile organic compounds (VOCs) can be considered as DAMPs. Due to their chemical nature, VOCs are supposed to act not only locally and systemically in the same plant but also between plants. Here, we focus on damage-induced volatiles (DIVs) that might be regarded as DAMPs; we will review their origin, chemical nature, physiochemical properties, biological relevance and putative function in plant-plant communications. Moreover, we discuss the possibility to use such airborne DAMPs as eco-friendly compounds to stimulate natural defenses in agriculture in order to avoid pesticides.

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Plants have evolved sophisticated defense mechanisms to overcome their sessile nature. However, if and how volatiles from cold-stressed plants can trigger interplant communication is still unknown. Here, we provide the first evidence for interplant communication via inducible volatiles in cold stress. The volatiles, including nerolidol, geraniol, linalool, and methyl salicylate, emitted from cold-stressed tea plants play key role(s) in priming cold tolerance of their neighbors via a C-repeat-binding factors-dependent pathway. The knowledge will help us to understand how plants respond to volatile cues in cold stress and agricultural ecosystems.

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MAIN CONCLUSION: Salinity alters VOC profile in emitter sweet basil plants. Airborne signals by emitter plants promote earlier flowering of receivers and increase their reproductive success under salinity. Airborne signals can prime neighboring plants against pathogen and/or herbivore attacks, whilst little is known about the possibility that volatile organic compounds (VOCs) emitted by stressed plants alert neighboring plants against abiotic stressors. Salt stress (50 mM NaCl) was imposed on Ocimum basilicum L. plants (emitters, namely NaCl), and a putative alerting-priming interaction was tested on neighboring basil plants (receivers, namely NaCl-S). Compared with the receivers, the NaCl plants exhibited reduced biomass, lower photosynthesis, and changes in the VOC profile, which are common early responses of plants to salinity. In contrast, NaCl-S plants had physiological parameters similar to those of nonsalted plants (C), but exhibited a different VOC fingerprint, which overlapped, for most compounds, with that of emitters. NaCl-S plants exposed later to NaCl treatment (namely NaCl-S + NaCl) exhibited changes in the VOC profile, earlier plant senescence, earlier flowering, and higher seed yield than C + NaCl plants. This experiment offers the evidence that (1) NaCl-triggered VOCs promote metabolic changes in NaCl-S plants, which, finally, increase reproductive success and (2) the differences in VOC profiles observed between emitters and receivers subjected to salinity raise the question whether the receivers are able to "propagate" the warning signal triggered by VOCs in neighboring companions.

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Plants produce and emit terpenes, including sesquiterpenes, during growth and development, which serve different functions in plants. The sesquiterpene nerolidol has health-promoting properties and adds a floral scent to plants. However, the glycosylation mechanism of nerolidol and its biological roles in plants remained unknown. Sesquiterpene UDP-glucosyltransferases were selected by using metabolites-genes correlation analysis, and its roles in response to cold stress were studied. We discovered the first plant UGT (UGT91Q2) in tea plant, whose expression is strongly induced by cold stress and which specifically catalyzes the glucosylation of nerolidol. The accumulation of nerolidol glucoside was consistent with the expression level of UGT91Q2 in response to cold stress, as well as in different tea cultivars. The reactive oxygen species (ROS) scavenging capacity of nerolidol glucoside was significantly higher than that of free nerolidol. Down-regulation of UGT91Q2 resulted in reduced accumulation of nerolidol glucoside, ROS scavenging capacity and tea plant cold tolerance. Tea plants absorbed airborne nerolidol and converted it to its glucoside, subsequently enhancing tea plant cold stress tolerance. Nerolidol plays a role in response to cold stress as well as in triggering plant-plant communication in response to cold stress. Our findings reveal previously unidentified roles of volatiles in response to abiotic stress in plants.

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The focus of this review is on how plants respond to combinations of multiple air pollutants. Global pollution trends, plant physiological responses and ecological perspectives in natural and agricultural systems are all discussed. In particular, we highlight the importance of studying sequential or simultaneous exposure of plants to pollutants, rather than exposure to individual pollutants in isolation, and explore how these responses may interfere with the way plants interact with their biotic community. Air pollutants can alter the normal physiology and metabolic functioning of plants. Here we describe how the phenotypic and molecular changes in response to multiple pollutants can differ compared to those elicited by single pollutants, and how different responses have been observed between plants in the field and in controlled laboratory conditions and between trees and crop plants. From an ecological perspective, we discuss how air pollution can result in greater susceptibility to biotic stressors and in direct or indirect effects on interactions with organisms that occupy higher trophic levels. Finally, we provide an overview of the potential uses of plants to mitigate air pollution, exploring the feasibility for pollution removal via the processes of bio-accumulation and phytoremediation. We conclude by proposing some new directions for future research in the field.

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BACKGROUND: Self-incompatible plants require simultaneous flowering mates for crosspollination and reproduction. Though the presence of flowering conspecifics and pollination agents are important for reproductive success, so far no cues that signal the flowering state of potential mates have been identified. Here, we empirically tested the hypothesis that plant floral volatiles induce flowering synchrony among self-incompatible conspecifics by acceleration of flowering and flower opening rate of non-flowering conspecifics. We exposed Brassica rapa Maarssen, a self-incompatible, in rather dense patches growing annual, to (1) flowering or non-flowering conspecifics or to (2) floral volatiles of conspecifics by isolating plants in separate containers with a directional airflow. In the latter, odors emitted by non-flowering conspecifics were used as control. RESULTS: Date of first bud, duration of first flower bud, date of first flower, maximum number of open flowers and flower opening rate were not affected by the presence of conspecific flowering neighbors nor by floral volatiles directly. CONCLUSIONS: This study presents a compelling approach to empirically test the role of flower synchronization by floral volatiles and challenges the premises that are underlying this hypothesis. We argue that the life history of the plant as well as its interaction with pollinators and insect herbivores, as well as the distance over which volatiles may serve as synchronization cue, set constraints on the fitness benefits of synchronized flowering which needs to be taken into account when testing the role of floral volatiles in synchronized flowering.

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Increased plant genotypic diversity in crop fields can promote ecosystem services including pest control, but understanding of mechanisms behind herbivore population responses to cultivar mixtures is limited. We studied aphid settling on barley plants exposed to volatiles from different cultivars, aphid population development in monocultures and two-cultivar mixtures, and differences in volatile composition between studied cultivars. Aphid responses to one cultivar in a mixture were neighbor-specific and this was more important for pest suppression than the overall mixture effect, aphid colonization patterns, or natural enemy abundance. Aphid populations decreased most in a mixture where both cultivars showed a reduced aphid-plant acceptance after reciprocal volatile exposure in the laboratory, and reduced population growth compared to monocultures in the field. Our findings suggest that herbivore population responses to crop genotypic diversity can depend on plant-plant volatile interactions, which can lead to changes in herbivore response to individual cultivars in a mixture, resulting in slower population growth. The impact of plant-plant interaction through volatiles on associated herbivore species is rarely considered, but improved understanding of these mechanisms would advance our understanding of the ecological consequences of biodiversity and guide development of sustainable agricultural practices. Combining cultivars in mixtures based on how they interact with each other is a promising strategy for sustainable pest management.

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