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Plants are capable of a range of complex interactions with the environment. Over the last decade, some authors have used this as evidence to argue that plants are cognitive agents. While there is no consensus on this view, it is certainly interesting to approach the debate from a comparative perspective, trying to understand whether different lineages of plants show different degrees of responsiveness to environmental cues, and how their responses compare with those of animals or humans. In this paper, I suggest that a potentially fruitful approach to these comparative studies is provided by automata theory. Accordingly, I shall present a possible application of this theory to plant communication. Two tentative results will emerge. First, that different lineages may exhibit different levels of complexity in response to similar stimuli. Second, that current evidence does not allow to infer great cognitive sophistication in plants.

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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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Plants display various forms of phenotypic plasticity in anticipation of changing conditions, many of which are influenced by information obtained from neighbouring plants. Here, we tested the hypothesis that cleistogamic Lamium amplexicaule plants can adaptively modify production of chasmogamous (CH) and cleistogamous (CL) flowers based on the perception of conspecific neighbours. The production and proportion of CH and CL flowers was examined in individual L. amplexicaule grown at varying densities or treated with root leachates from plants grown at different densities. When growing at high density or treated with root leachates from high-density pots, L. amplexicaule increased production of more expensive, potentially outcrossing CH flowers. In contrast, single plants or plants treated with root leachates from empty pots or single-source plants predominantly developed cheaper, self-pollinated CL flowers. The results demonstrate a novel root-based neighbour-perception modality that enables plants to adaptively adjust production of CH and CL flowers in response to the presence of potential reproductive partners. Further research is needed to explore the broader ecological implications of this novel interplant cueing on reproductive bet-hedging and plasticity in natural settings, as well as to identify the involved cues and their mode of operation.

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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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Volatile organic compounds mediate plant-to-plant communication, and plants receiving volatile cues can acquire greater defenses against attackers. It has been expected that volatiles are received by factors that eventually lead to the induction of defense-related gene expression; however, the nature of these factors remain unclear. Structure-activity relationship analysis of gene expression induction by volatiles should provide insights into the nature of these factors. We conducted a structure-activity relationship study using maize seedlings and (Z)-3-hexen-1-yl acetate (Z3HAC) as the lead compound. The acid portion of Z3HAC was not essential, and (Z)-3-hexen-1-ol (Z3HOL), which is formed after the hydrolysis of Z3HAC, is likely the structure essential for the upregulation of the genes. The double bond of Z3HOL is essential; however, its geometry is indistinguishable. Strict specificity was detected regarding the length of the methylene chain on the α- and ω-sides of the double bond, and therefore, the 3-hexen-1-ol structure was found to be the ultimate structure. This finding provides insight into the nature of the factors that interact with a volatile compound and subsequently activate signaling pathways, leading to the upregulation of a subset of defense genes.

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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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Trichoderma is a genus of filamentous fungi widely studied and used as a biological control agent in agriculture. However, its ability to form fungal networks for inter-plant communication by means of the so-called inter-plant "wired communication" has not yet been addressed. In our study we used the model plant Arabidopsis thaliana, the fungus Trichoderma hamatum (isolated from Brassicaceae plants) and the pathogens Sclerotinia sclerotiorum and Xanthomonas campestris (necrotrophic fungus and hemibiotrophic bacteria, respectively). We performed different combinations of isolated/neighboring plants and root colonization/non-colonization by T. hamatum, as well as foliar infections with the pathogens. In this way, we were able to determine how, in the absence of T. hamatum, there is an inter-plant communication that induces systemic resistance in neighboring plants of plants infected by the pathogens. On the other hand, the plants colonized by T. hamatum roots show a greater systemic resistance against the pathogens. Regarding the role of T. hamatum as an inter-plant communicator, it is the result of an increase in foliar signaling by jasmonic acid (increased expression of LOX1 and VSP2 genes and decreased expression of ICS1 and PR-1 genes), antagonistically increasing root signaling by salicylic acid (increased expression of ICS1 and PR-1 genes and decreased expression of LOX1 and VSP2). This situation prevents root colonization by T. hamatum of the foliarly infected plant and leads to massive colonization of the neighboring plant, where jasmonic acid-mediated systemic defenses are induced.

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Stressed plants show altered phenotypes, including changes in color, smell, and shape. Yet, airborne sounds emitted by stressed plants have not been investigated before. Here we show that stressed plants emit airborne sounds that can be recorded from a distance and classified. We recorded ultrasonic sounds emitted by tomato and tobacco plants inside an acoustic chamber, and in a greenhouse, while monitoring the plant's physiological parameters. We developed machine learning models that succeeded in identifying the condition of the plants, including dehydration level and injury, based solely on the emitted sounds. These informative sounds may also be detectable by other organisms. This work opens avenues for understanding plants and their interactions with the environment and may have significant impact on agriculture.

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Plants readily communicate with their pollinators, herbivores, symbionts, and the predators and pathogens of their herbivores. We previously demonstrated that plants could exchange, relay, and adaptively utilize drought cues from their conspecific neighbors. Here, we studied the hypothesis that plants can exchange drought cues with their interspecific neighbors. Triplets of various combinations of split-root Stenotaphrum secundatum and Cynodon dactylon plants were planted in rows of four pots. One root of the first plant was subjected to drought while its other root shared its pot with one of the roots of an unstressed target neighbor, which, in turn, shared its other pot with an additional unstressed target neighbor. Drought cuing and relayed cuing were observed in all intra- and interspecific neighbor combinations, but its strength depended on plant identity and position. Although both species initiated similar stomatal closure in both immediate and relayed intraspecific neighbors, interspecific cuing between stressed plants and their immediate unstressed neighbors depended on neighbor identity. Combined with previous findings, the results suggest that stress cuing and relay cuing could affect the magnitude and fate of interspecific interactions, and the ability of whole communities to endure abiotic stresses. The findings call for further investigation into the mechanisms and ecological implications of interplant stress cuing at the population and community levels.

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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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BACKGROUND: Oxathiapiprolin (OXPT; FRAC code 49) is a new piperidinyl-thiazole isooxazoline anti-oomycete fungicide that targets oxysterol-binding proteins. The fungicide is known to translocate acropetally from root to shoot to protect plants against fungal attack. RESULTS: OXPT is ambimobile. It can also translocate basipetally from shoot to root. OXPT exhibits an unprecedented capacity for trans-plant protection. When two tomato plants are grown in one pot, and one is treated with OXPT (on the stem, leaves or apex), while the other plant and soil surface are adequately covered, both plants become protected against late blight caused by Phytophthora infestans. CONCLUSION: Trans-plant systemic protection induced by OXPT involves translocation of the fungicide from the shoot of the treated plant to its root, exudation into the soil and uptake by the root of the neighboring untreated plant to protect it against the disease. Liquid chromatography-tandem mass spectrometry analyses confirmed the occurrence of OXPT in root exudates of OXPT-treated tomato plants in quantities sufficient to protect detached tomato leaves and intact plants against P. infestans. © 2022 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

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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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MAIN CONCLUSIONS: C. campestris parasitisation increases internal host defences at the expense of environmentally directed ones in the host species A. campestris, thus limiting plant defence against progressive parasitisation. Cuscuta campestris Yunck is a holoparasitic species that parasitises wild species and crops. Among their hosts, Artemisia campestris subsp. variabilis (Ten.) Greuter is significantly affected in natural ecosystems. Limited information is available on the host recognition mechanism and there are no data on the interactions between these species and the effects on the primary and specialised metabolism in response to parasitisation. The research aims at evaluating the effect of host-parasite interactions, through a GC-MS untargeted metabolomic analysis, chlorophyll a fluorescence, ionomic and δ13C measurements, as well as volatile organic compound (VOC) fingerprint in A. campestris leaves collected in natural environment. C. campestris parasitisation altered plant water status, forcing stomatal opening, stimulating plant transpiration, and inducing physical damages to the host antenna complex, thus reducing the efficiency of its photosynthetic machinery. Untargeted-metabolomics analysis highlighted that the parasitisation significantly perturbed the amino acids and sugar metabolism, inducing an increase in the production of osmoprotectants, which generally accumulate in plants as a protective strategy against oxidative stress. Notably, VOCs analysis highlighted a reduction in sesquiterpenoids and an increase in monoterpenoids levels; involved in plant defence and host recognition, respectively. Moreover, C. campestris induced in the host a reduction in 3-hexenyl-acetate, a metabolite with known repellent activity against Cuscuta spp. We offer evidences that C. campestris parasitisation increases internal host defences via primary metabolites at the expense of more effective defensive compounds (secondary metabolites), thus limiting A. campestris defence against progressive parasitisation.

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We have recently demonstrated that root cuing from drought-stressed plants increased the survival time of neighboring plants under drought, which came at performance costs under benign conditions. The involvement of abscisic acid (ABA) was implicated from additional experiments in which interplant drought cuing was greatly diminished in ABA-deficient plants. Here, we tested the hypothesis that ABA is the exogenous vector of interplant drought cuing. Pisum sativum plants were grown in rows of three split-root plants. One of the roots of the first plant was subjected to either drought of benign conditions in one rooting vial, while its other root shared its rooting vial with one of the roots of an unstressed neighbor, which in turn shared its other rooting vial with an additional unstressed neighbor. One hour after subjecting one of the roots of the first plant to drought, ABA concentrations were 106% and 145% higher around its other root and the roots of its unstressed neighbor, compared to their respective unstressed controls; however, the absolute concentrations of ABA found in the rooting media were substantially low. The results may indicate that despite its involvement in interplant drought and the commonly observed exchange of ABA between drought-stressed plants and their rhizospheres, ABA is not directly involved in exogenous interplant drought cuing. However, previous studies have shown that even minute concentrations of ABA in the rhizosphere can prevent ABA leakage from roots and thus to significantly increase endogenous ABA levels. In addition, under drought conditions, plants tend to accumulate ABA, which could markedly increase internal ABA concentrations over time and ABA concentrations in close proximity to the root surface might be significantly greater than estimated from entire rooting volumes. Finally, phaseic acid, an ABA degradation product, is known to activate various ABA receptors, which could enhance plant drought tolerance. It is thus feasible that while the role of ABA is limited, its more stable degradation products could play a significant role in interplant drought cuing. Our preliminary findings call for an extensive investigation into the identity and modes of operation of the exogenous vectors of interplant drought cuing.

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Light quality and chemicals in a plant's environment can provide crucial information about the presence and nature of antagonists, such as competitors and herbivores. Here, we evaluate the roles of three sources of information-shifts in the red:far red (R:FR) ratio of light reflected off of potentially competing neighbors, induced metabolic changes to damage by insect herbivores, and induced changes to volatile organic compounds emitted from herbivore-damaged neighboring plants-to affect metabolic responses in the tall goldenrod, Solidago altissima. We address the hypothesis that plants integrate the information available about competitors and herbivory to optimize metabolic responses to interacting stressors by exposing plants to the different types of environmental information in isolation and combination. We found strong interactions between the exposure to decreased R:FR light ratios and damage on the induction of secondary metabolites (volatile and non-volatile) in plants. Similarly, the perception of VOCs emitted from neighboring plants was altered by the simultaneous exposure to spectral cues from neighbors. These results suggest that plants integrate spectral and chemical environmental cues to change the production and perception of volatile and non-volatile compounds and highlight the role of plant context-dependent metabolic responses in mediating population and community dynamics.

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Plants have long been considered passive, static, and unchanging organisms, but this view is finally changing. More and more knowledge is showing that plants are aware of their surroundings, and they respond to a surprising variety of stimuli by modifying their growth and development. Plants extensively communicate with the world around them, above and below ground. Although communication through mycorrhizal networks and Volatile Organic Compounds has been known for a long time, acoustic perception and communication are somehow a final frontier of research. Perhaps surprisingly, plants not only respond to sound, they actually seem to emit sound as well. Roots emit audible clicks during growth, and sounds are emitted from xylem vessels, although the nature of these acoustic emissions still needs to be clarified. Even more interesting, there is the possibility that these sounds carry information with ecological implications, such as alerting insects of the hydration state of a possible host plant, and technological implications as well. Monitoring sound emissions could possibly allow careful monitoring of the hydration state of crops, which could mean significantly less water used during irrigation. This review summarizes the current knowledge on sound perception communication in plants and illustrates possible implications and technological applications.