Fungal Volatiles Research Articles

Volatiles from the fungal phytopathogen Penicillium aurantiogriseum modulate root metabolism and architecture through proteome resetting.

Volatile compounds (VCs) emitted by the fungal phytopathogen Penicillium aurantiogriseum promote root growth and developmental changes in Arabidopsis. Here we characterised the metabolic and molecular responses of roots to fungal volatiles. Proteomic analyses revealed that these compounds reduce the levels of aquaporins, the iron carrier IRT1 and apoplastic peroxidases. Fungal VCs also increased the levels of enzymes involved in the production of mevalonate (MVA)-derived isoprenoids, nitrogen assimilation and conversion of methionine to ethylene and cyanide. Consistently, fungal VC-treated roots accumulated high levels of hydrogen peroxide (H2 O2 ), MVA-derived cytokinins, ethylene, cyanide and long-distance nitrogen transport amino acids. qRT-PCR analyses showed that many proteins differentially expressed by fungal VCs are encoded by VC non-responsive genes. Expression patterns of hormone reporters and developmental characterisation of mutants provided evidence for the involvement of cyanide scavenging and enhanced auxin, ethylene, cytokinin and H2 O2 signalling in the root architecture changes promoted by fungal VCs. Our findings show that VCs from P. aurantiogriseum modify root metabolism and architecture, and improve nutrient and water use efficiencies through transcriptionally and non-transcriptionally regulated proteome resetting mechanisms. Some of these mechanisms are subject to long-distance regulation by photosynthesis and differ from those triggered by VCs emitted by beneficial microorganisms.

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

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

Roles of Fungal Volatiles from Perspective of Distinct Lifestyles in Filamentous Fungi.

Volatile compounds (VOCs) are not only media for communication within a species but also effective tools for sender to manipulate behavior and physiology of receiver species. Although the influence of VOCs on the interactions among organisms is evident, types of VOCs and specific mechanisms through which VOCs work during such interactions are only beginning to become clear. Here, we review the fungal volatile compounds (FVOCs) and their impacts on different recipient organisms from perspective of distinct lifestyles of the filamentous fungi. Particularly, we discuss the possibility that different lifestyles are intimately associated with an ability to produce a repertoire of FVOCs in fungi. The FVOCs discussed here have been identified and analyzed as relevant signals under a range of experimental settings. However, mechanistic insight into how specific interactions are mediated by such FVOCs at the molecular levels, amidst complex community of microbes and plants, requires further testing. Experimental designs and advanced technologies that attempt to address this question will facilitate our understanding and applications of FVOCs to agriculture and ecosystem management.

Screening of Fungi Isolated from the Brazilian Restinga for Insecticidal Activity

Research on microorganisms for the control of pests and pathogens is increasing. Such organisms display antagonistic effects on pests and pathogens, at the same time, they do not interfere with the sustainable development processes and are environmentally safe for human populations. Thus, bioprospection of fungi from restinga ecosystems is of interest as a novel source of microorganism and a yet unexplored source of chemical structures. This study selected endophytic fungi and fungi from the restinga soil samples to investigate their biological activity against insects. Fifty-three fungal isolates were used in screening bioassays against Atta sexdens rubropilosa leaf-cutting ant workers via direct contact of the insects with sporulating fungi cultures. This assay indicated that Trichoderma caused the highest mortality. Extracts from Trichoderma were then assessed for biological activity via ingestion, contact or exposure to fungal volatiles. Results showed that one Trichoderma sp. isolate (TR1) caused 50% mortality in 2, 1.5 and 4 days when ingested, sprayed onto the ants or by exposing ants to volatiles, respectively. Although this fungus is not known to be entomopathogenic, it could have potential use as an additional tool for pest control as it produces metabolites with antagonistic effects.

The Trichoderma atroviride Strains P1 and IMI 206040 Differ in Their Light-Response and VOC Production.

Trichoderma atroviride is a strong necrotrophic mycoparasite antagonizing and feeding on a broad range of fungal phytopathogens. It further beneficially acts on plants by enhancing growth in root and shoot and inducing systemic resistance. Volatile organic compounds (VOCs) are playing a major role in all those processes. Light is an important modulator of secondary metabolite biosynthesis, but its influence has often been neglected in research on fungal volatiles. To date, T. atroviride IMI 206040 and T. atroviride P1 are among the most frequently studied T. atroviride strains and hence are used as model organisms to study mycoparasitism and photoconidiation. However, there are no studies available, which systematically and comparatively analyzed putative differences between these strains regarding their light-dependent behavior and VOC biosynthesis. We therefore explored the influence of light on conidiation and the mycoparasitic interaction as well as the light-dependent production of VOCs in both strains. Our data show that in contrast to T. atroviride IMI 206040 conidiation in strain P1 is independent of light. Furthermore, significant strain- and light-dependent differences in the production of several VOCs between the two strains became evident, indicating that T. atroviride P1 could be a better candidate for plant protection than IMI 206040.

Plant responses to fungal volatiles involve global posttranslational thiol redox proteome changes that affect photosynthesis.

Microorganisms produce volatile compounds (VCs) that promote plant growth and photosynthesis through complex mechanisms involving cytokinin (CK) and abscisic acid (ABA). We hypothesized that plants' responses to microbial VCs involve posttranslational modifications of the thiol redox proteome through action of plastidial NADPH-dependent thioredoxin reductase C (NTRC), which regulates chloroplast redox status via its functional relationship with 2-Cys peroxiredoxins. To test this hypothesis, we analysed developmental, metabolic, hormonal, genetic, and redox proteomic responses of wild-type (WT) plants and a NTRC knockout mutant (ntrc) to VCs emitted by the phytopathogen Alternaria alternata. Fungal VC-promoted growth, changes in root architecture, shifts in expression of VC-responsive CK- and ABA-regulated genes, and increases in photosynthetic capacity were substantially weaker in ntrc plants than in WT plants. As in WT plants, fungal VCs strongly promoted growth, chlorophyll accumulation, and photosynthesis in ntrc-Δ2cp plants with reduced 2-Cys peroxiredoxin expression. OxiTRAQ-based quantitative and site-specific redox proteomic analyses revealed that VCs promote global reduction of the thiol redox proteome (especially of photosynthesis-related proteins) of WT leaves but its oxidation in ntrc leaves. Our findings show that NTRC is an important mediator of plant responses to microbial VCs through mechanisms involving global thiol redox proteome changes that affect photosynthesis.

Volatiles of pathogenic and non-pathogenic soil-borne fungi affect plant development and resistance to insects

Plants are ubiquitously exposed to a wide diversity of (micro)organisms, including mutualists and antagonists. Prior to direct contact, plants can perceive microbial organic and inorganic volatile compounds (hereafter: volatiles) from a distance that, in turn, may affect plant development and resistance. To date, however, the specificity of plant responses to volatiles emitted by pathogenic and non-pathogenic fungi and the ecological consequences of such responses remain largely elusive. We investigated whether Arabidopsis thaliana plants can differentiate between volatiles of pathogenic and non-pathogenic soil-borne fungi. We profiled volatile organic compounds (VOCs) and measured CO2 emission of 11 fungi. We assessed the main effects of fungal volatiles on plant development and insect resistance. Despite distinct differences in VOC profiles between the pathogenic and non-pathogenic fungi, plants did not discriminate, based on plant phenotypic responses, between pathogenic and non-pathogenic fungi. Overall, plant growth was promoted and flowering was accelerated upon exposure to fungal volatiles, irrespectively of fungal CO2 emission levels. In addition, plants became significantly more susceptible to a generalist insect leaf-chewing herbivore upon exposure to the volatiles of some of the fungi, demonstrating that a prior fungal volatile exposure can negatively affect plant resistance. These data indicate that plant development and resistance can be modulated in response to exposure to fungal volatiles.

Volatile organic compounds influence the interaction of the Eurasian spruce bark beetle (Ips typographus) with its fungal symbionts

Insects have mutualistic symbioses with a variety of microorganisms. However, the chemical signals that maintain these insect−microbe relationships are poorly known compared to those from insect−plant symbioses. The spruce bark beetle, Ips typographus, the most destructive forest pest in Europe, has a symbiotic relationship with several fungi that are believed to contribute to its successful invasion of Norway spruce. Here we tested the hypothesis that volatile organic compounds (VOCs) emitted from fungal symbionts could be cues for bark beetles to recognize and distinguish among members of its microbial community. Behavioral experiments with fungi showed that immature adults of I. typographus are attracted to food sources colonized by their fungal symbionts but not to saprophytic fungi and that this attraction is mediated by volatile cues. GC-MS measurements revealed that the symbionts emitted VOCs. Testing the activity of these compounds on beetle antennae using single sensillum recordings showed that beetles detect many fungal volatiles and possess olfactory sensory neurons specialized for these compounds. Finally, synthetic blends of fungal volatiles attracted beetles in olfactometer experiments. These findings indicate that volatile compounds produced by fungi may act as recognition signals for bark beetles to maintain specific microbial communities that might have impact on their fitness.

Tobacco Growth Promotion by the Entomopathogenic Fungus, Isaria javanica pf185

Isaria javanica pf185 is an important entomopathogenic fungus with potential for use as an agricultural biocontrol agent. However, the effect of I. javanica pf185 on plant growth is unknown. Enhanced tobacco growth was observed when tobacco roots were exposed to spores, cultures, and fungal cell-free culture supernatants of this fungus. Tobacco seedlings were also exposed to the volatiles of I. javanica pf185 in vitro using I-plates in which the plant and fungus were growing in separate compartments connected only by air space. The length and weight of seedlings, content of leaf chlorophyll, and number of root branches were significantly increased by the fungal volatiles. Heptane, 3-hexanone, 2,4-dimethylhexane, and 2-nonanone were detected, by solid-phase micro-extraction and gas chromatography-mass spectrophotometry, as the key volatile compounds produced by I. javanica pf185. These findings illustrate that I. javanica pf185 can be used to promote plant growth, and also as a biocontrol agent of insect and plant diseases. Further studies are necessary to elucidate the mechanisms by which I. javanica pf185 promotes plant growth.

Global Research Trends in Health Effects of Volatile Organic Compounds during the Last 16 Years: A Bibliometric Analysis

ABSTRACT In recent years, the health effects of volatile organic compounds (VOCs) have attracted increasing attention. However, there is no published literature conducting a bibliometric analysis to explore the tendency. The purpose of this study is to provide a bibliometric analysis of the research on the health effects of VOCs over the past 16 years. Based on the data retrieved from the Web of Science Core Collection database, several bibliometric indicators mainly including topics (keywords), journals, co-citation relationship, leading countries and institutions were evaluated. Among the 1,035 articles, the top three high-yield years were 2018 (n = 122), 2016 (n = 120), and 2017 (n = 105). Through co-citation analysis, TOP 10 clusters were obtained (respectively, BTEX, VOCs, indoor air, radon, indoor chemistry, VOC, photocatalytic oxidation, urinary metabolites of volatile organic compounds, fungal volatiles and nitrogen dioxide). Then, by constructing co-occurrence network of keywords, we revealed that “exposure” and “emissions” are two hotspots in the literature examined. Also, the results demonstrated that USA is the leading country (n = 294) and TSINGHUA UNIV. is the leading institution (n = 24). Moreover, the top three popular journals publishing the topic on health effects of VOCs were identified, respectively Atmos. Environ., Environ. Sci. Technol. and Indoor Air. Notably, in the literature examined, the most common diseases potentially associated with VOCs are mainly involved in the respiratory system, blood system and inflammation. Therefore, this study assessed publications on health effects of VOCs using bibliometric approaches, which provided the research status and trends of the topic and potential hints to future investigation in this field.

Volatile and non-volatile fungal oxylipins in fungus-invertebrate interactions

Abstract Eight-carbon volatiles are characteristic of the odour profile of many filamentous fungi. They derive from enzymatic or non-enzymatic lipid oxidation and are thus termed volatile oxylipins. Collectively, non-volatile and volatile fungal oxylipins are important hormone-like factors that regulate the phenotypic status of a fungus, i.e. growth, morphological differentiation and secondary metabolite production. Given this intimate link between oxylipin formation and phenotypic change, we propose that the release of volatile oxylipins is an important means by which fungi may influence the course and outcome of interactions with animals. Such invertebrate – fungus interactions are intricate inter–kingdom relationships where either one depends on the other, or both on each other, where one is to the others benefit or detriment – eventually having even consequences on third parties and thus influencing whole foodwebs. In this review, we first highlight the connections between oxylipin formation and fungal phenotypic changes, how they affect invertebrate interactions and vice versa. We then expand this by implementing eight-carbon volatiles as infochemicals. Infochemicals are cues or signals perceived by the invertebrates' chemical senses, that are to the invertebrates' or the fungus’ benefit or detriment, through the behavioural responses they elicit. We point out, with various examples, that there is a strong analogy between fungus-invertebrate interactions mediated by fungal eight-carbon volatiles and plant-herbivore interactions mediated by six-carbon green-leaf volatiles released from wounded or stressed plants.

Behavioral Responses of Pityophthorus juglandis (Coleoptera: Curculionidae: Scolytinae) to Volatiles of Black Walnut and Geosmithia morbida (Ascomycota: Hypocreales: Bionectriaceae), the Causal Agent of Thousand Cankers Disease.

Thousand cankers disease (TCD) is a pest complex formed by the association of the walnut twig beetle (WTB), Pityophthorus juglandis Blackman (Coleoptera: Curculionidae: Scolytinae), with the fungal pathogen Geosmithia morbida Kolařík, Freeland, Utley and Tisserat (Ascomycota: Hypocreales: Bionectriaceae). Current monitoring and detection efforts for WTB rely on a pheromone lure that is effective over a limited distance while plant- and fungal-derived volatiles that may facilitate host location remain poorly understood. In this study, we test the hypothesis that adult beetles are attracted to volatiles of black walnut, Juglans nigra L. (Juglandaceae), and the pathogen, G. morbida. We measured the response of beetles to head-space volatiles collected from leaves and stems of 12 genotypes of black walnut and found genotypic variation in the attractiveness of host trees to adult WTB. Volatile profiles of the most attractive genotypes contained more α-pinene and β-pinene, and adult beetles were attracted to both of these compounds in olfactometer bioassays. In bioassays, we also demonstrated that adult WTB are attracted to volatiles of G. morbida. These findings suggest that, in addition to the aggregation pheromone, dispersing WTB potentially use host plant and fungal volatiles to locate suitable larval hosts. Finally, we conducted a field experiment to determine the extent to which ethanol, a common attractant for bark beetles, and limonene, a known bark beetle repellent, influence the behavior of adult WTB to pheromone-baited traps. Although ethanol did not increase trap capture, WTB were repelled by limonene, suggesting that this compound could be used to manipulate and manage WTB populations.

Volatile compounds produced by Fusarium spp. isolated from Meloidogyne paranaensis egg masses and corticous root tissues from coffee crops are toxic to Meloidogyne incognita

Meloidogyne species produce egg masses containing nutrients which may serve as feeding substrate for rhizospheric fungi. In the present work we isolated fungi form Meloidogyne paranaensis egg masses. Amongst the fungi isolated 67% belonged to the genus Fusarium and, within those, 52% of the isolates were of the species F. oxysporum. Isolates from F. oxysporum and F. solani significantly reduced M. incognita infectivity and reproduction in tomato when J2 were exposed to fungal volatiles, causing up to 100% immobility in in vitro tests. Water exposed to the volatile compounds produced by fungi and mixed to the J2 suspension caused toxicity in M. incognita J2 and reduced infectivity and reproduction of nematodes inoculated in tomato, when compared to the control. Using gas chromatography-mass spectrometry (GC-MS), the volatile compounds produced by F. oxysporum and F. solani were identified and gathered in six main categories: esters, alcohols, phenols, aldehydes, carboxylic acids and sesquiterpenes, making up a total of 23 molecules. For the first time, 12 molecules from various chemical groups were identified in the water exposed to the volatiles from F. oxysporum and F. solani. A lower number of molecules were detected in the toxic water when compared with the vapors produced by fungi. Within these molecules, various have been already reported as having high nematicidal activity. Thus, F. oxysporum and F. solani fungi from M. paranaensis egg masses produce volatile compounds with antagonistic activity to M. incognita.

Volatile organic compounds from the interaction between Fusarium verticillioides and maize kernels as a natural repellents of Sitophilus zeamais

Maize kernels are exposed to Sitophilus zeamais attack and Fusarium verticillioides infestation during storage, which can result in product deterioration and economic losses. The objective of this study was to evaluate the involvement of the Volatile Organic Compounds (VOCs) emitted by the fungi-corn system in grain-insect interactions. Volatiles emitted by healthy maize kernels were different from those emitted by fungal infected kernels, with the latter being enriched by alcohols, ketones and sesquiterpenes, which were considered early indicators of fungal contamination. The results demonstrated that the kernels exposed to the fungal VOCs and their pure compounds (1-octen-3-ol and 3-octanol) were less attractive and less damaged by S. zeamais than controls. In addition to compound adsorption, other processes may have caused the protective effect of exposed kernels against insect damage. This is the first contribution of the role of the fungal volatiles on the behavior of S. zeamais, and could provide an important contribution to the conservation of stored grains and pest management and an early indicator of fungal contamination.

Responses of the ambrosia beetle Xylosandrus compactus (Coleoptera: Curculionidea: Scolytinae) to volatile constituents of its symbiotic fungus Fusarium solani (Hypocreales: Nectriaceae)

Xylosandrus compactus is a polyphagus pest that cultivates a symbiotic fungus Fusarium solani in tunnels of host plants for food and is a major threat to coffee production in East Africa. We hypothesized that the female X. compactus, which is the only sex capable of flying to attack its hosts, is attracted to volatiles from F. solani. We investigated responses of females to volatiles released by fungal cultures and bioactive components identified in the fungal volatiles. In Y-tube olfactometer assays, ~68% of females were attracted to volatiles emitted from F. solani over clean air. Bioactive compounds were identified in the fungal volatiles by coupled gas chromatography (GC)/electroantennographic detection (EAD) and GC/mass spectrometric analyses as methyl isovalerate and 2,3-butanediol. We also identified ethanol, a known attractant of X. compactus, using solid phase microextraction captured fungal volatiles analyzed by GC/MS. In field trapping trials, we compared captures of females in plastic bottle traps baited with a range of doses of methyl isovalerate, 2,3-butanediol, and blends of the two compounds, with similar traps baited with solvent only and ethanol. Females were caught by all the baited traps at all the concentrations tested except traps baited with solvent only. Trap captures were however 14–37-fold lower in traps baited with single components and the blends than those baited with ethanol. The possible use of these components as a tool for kairomonal monitoring of populations of X. compactus is discussed.

Orientation of Navel Orangeworm (Lepidoptera: Pyralidae) Larvae and Adults Toward Volatiles Associated With Almond Hull Split and Aspergillus flavus.

The navel orangeworm Amyelois transitella (Walker, 1863, Lepidoptera: Pyralidae), a pest of California tree nuts, is associated with the fungus Aspergillus flavus, and previous research suggests these species are facultative mutualists. Because navel orangeworm larvae exhibit improved performance on diets containing this fungus, orientation toward hostplants infected with A. flavus may be adaptive. We conducted behavioral assays to determine if larvae respond to chemical cues produced by almond hull split and fungal infection. In petri dish arenas, larvae showed a preference for 1-octen-3-ol and 2-phenylethanol, volatiles characteristic of damaged plants, as well as methanolic extracts of almond meal with 1-octen-3-ol and the fungal volatile conophthorin. In contrast, larvae displayed aversion to ethyl benzoate, an inhibitor of fungal growth. When we assessed oviposition behavior relative to substrates with and without A. flavus, females laid almost twice as many eggs near inoculated surfaces. Moreover, an average of 63% of eggs laid near inoculated substrates were fertilized, compared with 24% of eggs near uninoculated sites. We also tested the hypothesis that unfertilized eggs are laid on nutrient-poor substrates to provide supplemental nutrition for larvae in an assay comparing larval survivorship in the presence and absence of unfertilized eggs. Neonates given eggs survived 2.5 times longer on an average than unprovisioned neonates (208.8 h vs. 85.2 h), indicating that this species may compensate with cannibalism for oviposition on lower-quality food sources. We conclude that larvae orient to probable host plant and fungal volatiles associated with hull split and document a possible strategy for larvae to establish on low-quality hosts.

Fungal volatiles - a survey from edible mushrooms to moulds.

Covering: up to January 2017This review gives a comprehensive overview of the production of fungal volatiles, including the history of the discovery of the first compounds and their distribution in the various investigated strains, species and genera, as unravelled by modern analytical methods. Biosynthetic aspects and the accumulated knowledge about the bioactivity and biological functions of fungal volatiles are also covered. A total number of 325 compounds is presented in this review, with 247 cited references.

Bioactive Volatiles from an Endophytic Daldinia cf. concentrica Isolate Affect the Viability of the Plant Parasitic Nematode Meloidogyne javanica.

Plant-parasitic nematodes form one of the largest sources of biotic stress imposed on plants, and are very difficult to control; among them are the obligate parasites, the sedentary root-knot nematodes (RKNs)–Meloidogyne spp.–which are extremely polyphagous and exploit a very wide range of hosts. Endophytic fungi are organisms that spend most of their life cycle within plant tissue without causing visible damage to the host plant. Many endophytes secrete specialized metabolites and/or emit volatile organic compounds (VOCs) that exhibit biological activity. Recently, we demonstrated that the endophytic fungus Daldinia cf. concentrica secrets biologically active VOCs. Here we examined the ability of the fungus and its VOCs to control the RKN M. javanica both in vitro and greenhouse experiments. The D. cf. concentrica VOCs showed bionematicidal activity against the second-stage juveniles (J2s) of M. javanica. We found that exposure of J2s to fungal volatiles caused 67% reduction in viability, and that application of a synthetic volatile mixture (SVM), comprising 3-methyl-1-butanol, (±)-2-methyl-1-butanol, 4-heptanone, and isoamyl acetate, in volumetric ratio of 1:1:2:1 further reduced J2s viability by 99%. We demonstrated that, although each of the four VOCs significantly reduced the viability of J2s relative to the control, only 4-heptanone elicited the same effect as the whole mixture, with nematicidal activity of 90% reduction in viability of the J2s. Study of the effect of the SVM on egg hatching demonstrated that it decreased eggs hatching by 87%. Finally, application of the SVM to soil inoculated with M. javanica eggs or J2s prior to planting susceptible tomato plants resulted in a significantly reduced galling index and fewer eggs produced on each root system, with no effect on root weight. Thus, D. cf. concentrica and/or SVM based on fungal VOCs may be considered as a novel alternative approach to controlling the RKN M. javanica.

Fungal Volatiles Can Act as Carbon Sources and Semiochemicals to Mediate Interspecific Interactions Among Bark Beetle-Associated Fungal Symbionts.

Mountain pine beetle (Dendroctonus ponderosae) has killed millions of hectares of pine forests in western North America. Beetle success is dependent upon a community of symbiotic fungi comprised of Grosmannia clavigera, Ophiostoma montium, and Leptographium longiclavatum. Factors regulating the dynamics of this community during pine infection are largely unknown. However, fungal volatile organic compounds (FVOCs) help shape fungal interactions in model and agricultural systems and thus may be important drivers of interactions among bark beetle-associated fungi. We investigated whether FVOCs can mediate interspecific interactions among mountain pine beetle’s fungal symbionts by affecting fungal growth and reproduction. Headspace volatiles were collected and identified to determine species-specific volatile profiles. Interspecific effects of volatiles on fungal growth and conidia production were assessed by pairing physically-separated fungal cultures grown either on a carbon-poor or -rich substrate, inside a shared-headspace environment. Fungal VOC profiles differed by species and influenced the growth and/or conidia production of the other species. Further, our results showed that FVOCs can be used as carbon sources for fungi developing on carbon-poor substrates. This is the first report demonstrating that FVOCs can drive interactions among bark beetle fungal symbionts, and thus are important factors in beetle attack success.

Volatile Organic Compounds Emitted by Fungal Associates of Conifer Bark Beetles and their Potential in Bark Beetle Control.

Conifer bark beetles attack and kill mature spruce and pine trees, especially during hot and dry conditions. These beetles are closely associated with ophiostomatoid fungi of the Ascomycetes, including the genera Ophiostoma, Grosmannia, and Endoconidiophora, which enhance beetle success by improving nutrition and modifying their substrate, but also have negative impacts on beetles by attracting predators and parasites. A survey of the literature and our own data revealed that ophiostomatoid fungi emit a variety of volatile organic compounds under laboratory conditions including fusel alcohols, terpenoids, aromatic compounds, and aliphatic alcohols. Many of these compounds already have been shown to elicit behavioral responses from bark beetles, functioning as attractants or repellents, often as synergists to compounds currently used in bark beetle control. Thus, these compounds could serve as valuable new agents for bark beetle management. However, bark beetle associations with fungi are very complex. Beetle behavior varies with the species of fungus, the stage of the beetle life cycle, the host tree quality, and probably with changes in the emission rate of fungal volatiles. Additional research on bark beetles and their symbiotic associates is necessary before the basic significance of ophiostomatoid fungal volatiles can be understood and their applied potential realized.Electronic supplementary materialThe online version of this article (doi:10.1007/s10886-016-0768-x) contains supplementary material, which is available to authorized users.