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Spatial characteristics of volatile communication in lodgepole pine trees: Evidence of kin recognition and intra-species support

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Abstract

Plant interactions using volatile organic compounds, particularly in the context of kin recognition have received considerable attention in recent years, but several discrepancies and conflicting results have restricted our understanding. We propose that some of these discrepancies in literature are in part due to integral spatial characteristics of sites, and plant attributes. Chemotypic plasticity is commonly used to characterize kin, particularly in conifers. We studied constitutive and induced monoterpene chemotypes of non-attacked lodgepole pine trees within 30 m radii of pine trees attacked by mountain pine beetle. We tested the effects of volatile compounds emitted from the attacked trees on the non-attacked trees by challenge inoculations with a mountain pine beetle associated fungus. We found no relationship between constitutive monoterpene concentrations of the non-attacked trees and distance or direction from the attacked trees or site aspects. In contrast, the effects of volatile compounds were evident after inoculations, depending on distance from the attacked trees and site aspects. However, these interactions only emerged among chemotypically related trees. These results suggest that plants discriminate between chemical cues from kin and strangers, and the emitters likely aid only chemotypically related plants by emitting specific blends of volatiles that can only be deciphered by the receiving kin. These results further demonstrate the importance of incorporating spatial characteristics of sites and plant attributes in studies aimed at investigating intra-species interactions using volatile organic compounds.

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Plants may “eavesdrop” on volatile organic compounds (VOCs) released by herbivore-attacked neighbors to activate defenses before being attacked themselves. Transcriptome and signal cascade analyses of VOC-exposed plants suggest that plants eavesdrop to prime direct and indirect defenses and to hone competitive abilities. Advances in research on VOC biosynthesis and perception have facilitated the production of plants that are genetically “deaf” to particular VOCs or “mute” in elements of their volatile vocabulary. Such plants, together with advances in VOC analytical instrumentation, will allow researchers to determine whether fluency enhances the fitness of plants in natural communities.
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Plants can defend themselves to pathogen and herbivore attack by responding to chemical signals that are emitted by attacked plants. It is well established that such signals can be transferred through the air. In theory, plants can also communicate with each other through underground common mycorrhizal networks (CMNs) that interconnect roots of multiple plants. However, until now research focused on plant-to-plant carbon nutrient movement and there is no evidence that defense signals can be exchanged through such mycorrhizal hyphal networks. Here, we show that CMNs mediate plant-plant communication between healthy plants and pathogen-infected tomato plants (Lycopersicon esculentum Mill.). After establishment of CMNs with the arbuscular mycorrhizal fungus Glomus mosseae between tomato plants, inoculation of 'donor' plants with the pathogen Alternaria solani led to increases in disease resistance and activities of the putative defensive enzymes, peroxidase, polyphenol oxidase, chitinase, β-1,3-glucanase, phenylalanine ammonia-lyase and lipoxygenase in healthy neighbouring 'receiver' plants. The uninfected 'receiver' plants also activated six defence-related genes when CMNs connected 'donor' plants challenged with A. solani. This finding indicates that CMNs may function as a plant-plant underground communication conduit whereby disease resistance and induced defence signals can be transferred between the healthy and pathogen-infected neighbouring plants, suggesting that plants can 'eavesdrop' on defence signals from the pathogen-challenged neighbours through CMNs to activate defences before being attacked themselves.
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Host-plants can mediate the interactions between herbivores and their mutualists and also between parasitic plants and their mutualists. The present study reveals how a hemiparasitic plant parasitizing three host species gives rise to three distinct hemiparasite-host neighborhoods which differ in terms of volatile composition and pollinator attractiveness. The study was performed in a population of the mistletoe Tristerix verticillatus infecting three different species of hosts occurring in sympatry within a small area, thus exposing all individuals studied to similar abiotic conditions and pollinator diversity; we assessed the effect of hosts on the hemiparasites' visual and olfactory cues for pollinator attraction. During the study period, the hemiparasite individuals were flowering but the hosts were past their flowering stage. We collected volatile organic compounds from the hemiparasite and its hosts, measured floral display characteristics and monitored bird and insect visitors to inflorescences of T. verticillatus. We showed that: (1) floral patches did not differ in terms of floral display potentially involved in the attraction of pollinators, (2) hosts and hemiparasites on each host were discriminated as distinct chemical populations in terms of their volatile chemical profiles, (3) insect visitation rates differed between hemiparasites parasitizing different hosts, and (4) volatile compounds from the host and the hemiparasite influenced the visitation of hemiparasite flowers by insects. The study showed that a species regarded as "ornithophilic" by its floral morphology was actually mostly visited by insects that interacted with its sexual organs during their visits and carried its pollen, and that host-specific plant-volatile profiles within the T. verticillatus population were associated with differential attractiveness to pollinating insects.
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In spite of initial doubts about the reality of 'talking trees', plant resistance expression mediated by volatile compounds that come from neighboring plants is now well described. Airborne signals usually improve the resistance of the receiver, but without obvious benefits for the emitter, thus making the evolutionary explanation of this phenomenon problematic. Here, we discuss four possible non-exclusive explanations involving the role of volatiles: in direct defense, as within-plant signals, as traits that synergistically interact with other defenses, and as cues among kin. Unfortunately, there is a lack of knowledge on the fitness consequences of plant communication for both emitter and receiver. This information is crucial to understanding the ecology and evolution of plant communication via airborne cues.
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Millions of hectares of lodgepole pine trees have been affected by the recent mountain pine beetle outbreaks, which also left significant numbers of live host trees in some areas. Studies have primarily focused on the changes of forest conditions in post-outbreak stands, but whether such changes impact the growth, defense, and their interactions of residual pine trees is generally unknown. In this study, we compared the growth-defense relationship of lodgepole pine trees between pre- and post-outbreak periods by examining annual radial growth rates and xylem resin duct characteristics. We also tested the effects of varying percent host tree mortality and forest stand density on the growth-defense relationship of residual pine trees. We found that resin duct densities of residual pine trees were higher and resin ducts occupied larger areas in the xylem in post-outbreak period than in pre-outbreak period. Following outbreak, the percent host mortality showed a positive relationship with the resin duct density of all healthy residual trees, while stand density did not impact any of the resin duct characteristics. We conclude that bark beetle outbreaks can alter the growth, defense, and their interactions of residual pine trees, especially in stands with greater levels of pine mortality. This study also provides an empirical evidence, suggesting that residual trees might be more resistant to future bark beetle attacks.
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Mountain pine beetle (MPB) has recently invaded jack pine forests in western Canada. This invasion signifies a climate change‐induced range expansion by a native insect. The mechanism underlying this invasion is unknown, but likely involves phytochemicals that play critical roles in MPB biology. Thus far, studies have investigated the compatibility of jack pine chemistry with beetles and their microbial symbionts. I have identified three phytochemical mechanisms that have likely facilitated the host range expansion of MPB. First, jack pine chemistry is overall similar to that of the historical hosts of MPB. In particular, jack pine chemistry is compatible with beetle pheromone production, aggregation on host trees and larval development. Furthermore, the compatibility of jack pine chemistry maintains beneficial interactions between MPB and its microbial symbionts. Second, compared with historical hosts, the novel host not only has lower concentrations of toxic and repellent defense chemicals, but also contains large concentrations of chemicals promoting host colonization by MPB. These patterns are especially pronounced when comparing novel hosts with well‐defended historical hosts. Finally, before MPBs arrived in jack pine forests, they invaded a zone of hybrids of novel and historical hosts that likely improved beetle success on jack pine, as hybrids show chemical characteristics of both hosts. In conclusion, the phytochemistry of jack pine has likely facilitated the biological invasion of this novel host by MPB.
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Although cooperative interactions among kin have been established in a variety of biological systems, their occurrence in plants remains controversial.Plants of Arabidopsis thaliana were grown in rows of either a single or multiple accessions.Plants recognized kin neighbours and horizontally reoriented leaf growth, a response not observed when plants were grown with nonkin. Plant kin recognition involved the perception of the vertical red/far-red light and blue light profiles. Disruption of the light profiles, mutations at the PHYTOCHROME B, CRYPTOCHROME 1 or 2, or PHOTOTROPIN 1 or 2 photoreceptor genes or mutations at the TRYPTOPHAN AMINOTRANSFERASE OF ARABIDOPSIS1 gene required for auxin (growth hormone) synthesis impaired the response. The leaf-position response increases plant self-shading, decreases mutual shading between neighbours and increases fitness.Light signals from neighbours are known to shape a more competitive plant body. Here we show that photosensory receptors mediate cooperative rather than competitive interactions among kin neighbours by reducing the competition for local pools of resources.
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Host plant secondary chemistry can have cascading impacts on host and range expansion of herbivorous insect populations. We investigated the role of host secondary compounds on pheromone production by the mountain pine beetle (Dendroctonus ponderosae) (MPB) and beetle attraction in response to a historical (lodgepole pine, Pinus contorta var. latifolia) and a novel (jack pine, Pinus banksiana) hosts, as pheromones regulate the host colonization process. Beetles emit the same pheromones from both hosts, but more trans-verbenol, the primary aggregation pheromone, was emitted by female beetles on the novel host. The phloem of the novel host contains more a-pinene, a secondary compound that is the precursor for trans-ver-benol production in beetle, than the historical host. Beetle-induced emission of 3-carene, another secondary compound found in both hosts, was also higher from the novel host. Field tests showed that the addition of 3-carene to the pheromone mixture mimicking the aggrega-tion pheromones produced from the two host species increased beetle capture. We conclude that chemical similarity between historical and novel hosts has facilitated host expansion of MPB in jack pine forests through the exploitation of common host secondary compounds for pheromone production and aggregation on the hosts. Furthermore, broods emerging from the novel host were larger in terms of body size.
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Volatile communication between plants causing enhanced defence has been controversial. Early studies were not replicated, and influential reviews questioned the validity of the phenomenon. We collected 48 well-replicated studies and found overall support for the hypothesis that resistance increased for individuals with damaged neighbours. Laboratory or greenhouse studies and those conducted on agricultural crops showed stronger induced resistance than field studies on undomesticated species, presumably because other variation had been reduced. A cumulative analysis revealed that early, non-replicated studies were more variable and showed less evidence for communication. Effects of habitat and plant growth form were undetectable. In most cases, the mechanisms of resistance and alternative hypotheses were not considered. There was no indication that some response variables were more likely to produce large effects. These results indicate that plants of diverse taxonomic affinities and ecological conditions become more resistant to herbivores when exposed to volatiles from damaged neighbours.
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Plants emit a diverse array of phytogenic volatile organic compounds (VOCs). The production and emission of VOCs has been an important area of research for decades. However, recent research has revealed the importance of VOC catabolism by plants and VOC degradation in the atmosphere for plant growth and survival. Specifically, VOC catabolism and degradation have implications for plant C balance, tolerance to environmental stress, plant signaling, and plant-atmosphere interactions. Here we review recent advances in our understanding of VOC catabolism and degradation, propose experiments for investigating VOC catabolism, and suggest ways to incorporate catabolism into VOC emission models. Improving our knowledge of VOC catabolism and degradation is crucial for understanding plant metabolism and predicting plant survival in polluted environments.
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Communication between plants has not been widely accepted by most ecologists. However, recent field experiments indicated that wild tobacco plants became more resistant to herbivores when grown in close proximity to clipped sagebrush neighbors. Tobacco plants grown within 15cm of sagebrush that had been either manually clipped with scissors or damaged by herbivores experienced less naturally occurring folivory than tobacco plants with unclipped neighbors. These results were consistent over five field seasons and involved treatments that were randomly assigned and well replicated. Associated with lower levels of herbivory were increased activities of polyphenol oxidase in tobacco foliage near clipped sagebrush neighbors. Experiments that blocked either air or soil contact between sagebrush and tobacco indicated that the communication was airborne rather than soilborne. Alternative explanations involving altered microenvironmental conditions or avoidance of clipped sagebrush by herbivores were not supported.Much remains to be learned about the natural history of this phenomenon. Apparently the plants must be in close proximity for communication to occur. Preliminary results suggest that communication between sagebrush and other plants may also occur. The mechanisms of communication as well as its ecological and evolutionary significance remain unknown.
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Monoterpene analysis was carried out on the shoot cortical oleoresin of natural stands of Lodgepole pine sampled across an extensive part of its range in North America. The geographical variation in monoterpene composition was similar to that which had been previously deduced from analysis of planted origins grown in Britain from seed collected in North America. The independence of the monoterpene composition on the planting site was further shown by analysis of a number of trees grown in Sweden. Origins from the northern parts of the natural range showed that the biochemical region based on the Rocky Mountains extended northwards to north-east British Columbia and into the Yukon. Monoterpene data showed populations from this region to be characterized by unusually high variation in the biochemical genotypes encountered, and locally to show evidence of a close genetic relationship with Jack pine.
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If carbon (C) sinks withdraw carbohydrates as they are transported along tree stems, carbohydrate availability may depend on local sink strength and distance from sources. Defenses, including monoterpenes - a major component of resin - limit the invasibility of pines. Since carbohydrate reserves fund monoterpene synthesis, we hypothesized that monoterpene concentrations in pine stems would decrease from the crown to the lower stem, and susceptibility to fungal infection would increase. Here, we measured carbohydrate and monoterpene concentrations along the stems of lodgepole pine trees (Pinus contorta var. latifolia) before inoculating with a blue-stain fungus at different heights. After 6 wk, we assessed tree responses to fungal infection based on lesion length and carbohydrate mobilization. Concentrations of carbohydrates and monoterpenes in the phloem before inoculation decreased with distance from the crown, whereas lesion lengths after inoculation increased. However, trees mobilized sugars in response to fungal infection such that carbohydrate reserves near lesions were similar at all heights. Despite C mobilization, the lower stem was more vulnerable than the upper stem. Consistent with predictions based on sink-source relationships, vulnerability occurred where carbohydrates were less available, and likely resulted from C withdrawal by sinks higher in the supply chain.
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An official journal of the Genetics Society, Heredity publishes high-quality articles describing original research and theoretical insights in all areas of genetics. Research papers are complimented by News & Commentary articles and reviews, keeping researchers and students abreast of hot topics in the field.
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Summary • The ability of arbuscular mycorrhizal (AM) networks originating from plants of different species, genera and families to become interconnected by means of hyphal anastomoses was assessed. • An in vivo two-dimensional experimental model system was used to reveal the occurrence of linkages between contiguous mycorrhizal networks spreading from Allium porrum root systems and those originating from Daucus carota, Gossypium hirsutum, Lactuca sativa, Solanum melongena, colonized by Glomus mosseae. • Percentages of hyphal contacts leading to anastomosis between extraradical networks originating from different plant species ranged from 44% in the pairing A. porrum–S. melongena to 49% in A. porrum–G. hirsutum. DAPI and Sytox stainings detected nuclei in the middle of fusion bridges connecting different mycorrhizal networks. • Present data suggest that, by means of anastomoses, AM fungal mycelium would potentially create an indefinitely large network interconnecting different plants in a community, and that, in the absence of sexual recombination, the intermingling of nuclei in extraradical mycelium may provide endless opportunities for the exchange of genetic material. ©New Phytologist (2004) doi: 10.1111/j.1469-8137.2004.01145.x New Phytologist (2004)
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Greenbeards are genes that can identify the presence of copies of themselves in other individuals, and cause their bearer to behave nepotistically toward those individuals. In recent years, a number of examples have been discovered, and it has been suggested that greenbeards represent one of the fundamental routes to social behaviors such as cooperation. However, despite their possible theoretical and empirical importance, many basic aspects of greenbeard biology are commonly misunderstood. Here, we distinguish between four different types of greenbeard, which differ in their evolutionary dynamics. We show that all four types exist, and that they differ in the ease with which they can be empirically detected. We clarify the inclusive fitness explanation of greenbeards, and show that they are not intragenomic outlaws. Finally, we argue that although greenbeards are likely to be most common and easiest to detect in microorganisms, they are unlikely to important in organisms such as humans.
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As an emerging subdiscipline of forest biology, canopy science has undergone a transition from observational, 'oh-wow' exploration to a more hypothesis-driven, experimental arena for rigorous field biology. Although efforts to explore forest canopies have occurred for a century, the new tools to access the treetops during the past 30 yr facilitated not only widespread exploration but also new discoveries about the complexity and global effects of this so-called 'eighth continent of the planet'. The forest canopy is the engine that fixes solar energy in carbohydrates to power interactions among forest components that, in turn, affect regional and global climate, biogeochemical cycling and ecosystem services. Climate change, biodiversity conservation, fresh water conservation, ecosystem productivity, and carbon sequestration represent important components of forest research that benefit from access to the canopy for rigorous study. Although some canopy variables can be observed or measured from the ground, vertical and horizontal variation in environmental conditions and processes within the canopy that determine canopy-atmosphere and canopy-forest floor interactions are best measured within the canopy. Canopy science has matured into a cutting-edge subset of forest research, and the treetops also serve as social and economic drivers for sustainable communities, fostering science education and ecotourism. This interdisciplinary context of forest canopy science has inspired innovative new approaches to environmental stewardship, involving diverse stakeholders.
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This special issue on "Chemical information transfer between wounded and unwounded plants" provides an overview of past and ongoing experiments on plant-to-plant communication. Since the studies on plant responses to single gaseous compounds were not particularly emphasised, the actual number of studies relevant to the subject is underestimated. All in all, we think the amount of data on damage-induced plant-to-plant information transfer makes that the phenomenon can no longer be denied and deserves intensified attention by the scientific community. In this epilogue we highlight a couple of issues which received little attention and present some speculative ideas. First we concentrate on functional aspects of plant-plant communication we stress the concept of damage-induced signalling as an ecological cost to the signal-sending plant and we discuss the theoretical development on interplant signalling, which is still in its infancy. With respect to mechanisms, we compare above- to belowground signalling, discuss potential cues and stress the possibility that responses in signal-exposed plants may be hidden. Finally, we address some future prospects which may help in the further development of the still underexposed phenomenon of damage-induced plant-to-plant information transfer.