Fungal Volatiles Research Articles

The relative abundances of yeasts attractive to Drosophila suzukii differ between fruit types and are greatest on raspberries

Fungal metabolic volatiles attract Drosophila suzukii which oviposits in ripening fruits, but there are few data describing the fungal microbiomes of commercial fruits susceptible to this insect pest. We tested the hypothesis that fruit type and ripening stage have a significant effect on fruit surface fungal communities using DNA metabarcoding approaches and found strong support for differences in all three fungal community biodiversity metrics analysed (numbers, types, and abundances of taxa). There was an average fivefold greater difference in fungal communities between sites with different fruit types (strawberry, cherry, raspberry, and blueberry) than across fruit developmental stages, demonstrating site and/or fruit type is the greater factor defining fungal community assemblage. The addition of a fungal internal standard (Plectosphaerella cucumerina) showed cherry had relatively static fungal populations across ripening. Raspberry had a greater prevalence of Saccharomycetales yeasts attractive to D. suzukii, including Hanseniaspora uvarum, which aligns with reports that raspberry is among the fruits with greatest susceptibility and attraction to D. suzukii. Greater knowledge of how yeast communities change during fruit maturation and between species or sites may be valuable for developing methods to manipulate fruit microbiomes for use in integrated pest management strategies to control D. suzukii.

Behavioural Responses of Male Aedes albopictus to Different Volatile Chemical Compounds.

Simple SummaryMany studies have been performed to assess the effects of chemical compounds on mosquito behaviour. These studies almost exclusively involve only female mosquitoes as they can transmit disease pathogens, or at least, cause biting nuisance. Few studies have considered male mosquitoes. The identification of chemical substances that attract males can be very useful for trapping purposes, especially for monitoring the makeup of the male population during control programmes, such as those involving the release of sterile male mosquitoes. Twenty-eight chemical compounds from different chemical classes were evaluated using a dual-port olfactometer assay with at least three serial hexane dilutions against a hexane control. The compounds included known animal, plant and fungal volatiles, and the components of a putative Aedes aegypti pheromone. Many of the compounds were repellent for male mosquitoes, especially at the highest concentration. One compound, decanoic acid, acted as an attractant for males at an intermediate concentration. Decanoic acid did not elicit a significant response from female mosquitoes.The Asian tiger mosquito, Aedes albopictus, has become one of the most important invasive vectors for disease pathogens such as the viruses that cause chikungunya and dengue. Given the medical importance of this disease vector, a number of control programmes involving the use of the sterile insect technique (SIT) have been proposed. The identification of chemical compounds that attract males can be very useful for trapping purposes, especially for monitoring the makeup of the male population during control programmes, such as those involving the use of the SIT. Twenty-eight chemical compounds from different chemical classes were evaluated using a dual-port olfactometer assay. The compounds included known animal, fungal and plant host volatiles, and components of a putative Aedes aegypti pheromone. Many of the compounds were repellent for male mosquitoes, especially at the highest concentration. One compound, decanoic acid, acted as an attractant for males at an intermediate concentration. Decanoic acid did not elicit a significant response from female mosquitoes.

Plant Growth Promotion by Two Volatile Organic Compounds Emitted From the Fungus Cladosporium halotolerans NGPF1.

Microbial volatiles have beneficial roles in the agricultural ecological system, enhancing plant growth and inducing systemic resistance against plant pathogens without being hazardous to the environment. The interactions of plant and fungal volatiles have been extensively studied, but there is limited research specifically elucidating the effects of distinct volatile organic compounds (VOCs) on plant growth promotion. The current study was conducted to investigate the impact of VOCs from Cladosporium halotolerans NGPF1 on plant growth, and to elucidate the mechanisms for the plant growth-promoting (PGP) activity of these VOCs. The VOCs from C. halotolerans NGPF1 significantly promoted plant growth compared with the control, and this PGP activity of the VOCs was culture medium-dependent. Headspace solid-phase microextraction (HS-SPME) coupled with gas chromatography–mass spectrometry (GC–MS) identified two VOC structures with profiles that differed depending on the culture medium. The two compounds that were only produced in potato dextrose (PD) medium were identified as 2-methyl-butanal and 3-methyl-butanal, and both modulated plant growth promotion and root system development. The PGP effects of the identified synthetic compounds were analyzed individually and in blends using N. benthamiana plants. A blend of the two VOCs enhanced growth promotion and root system development compared with the individual compounds. Furthermore, real-time PCR revealed markedly increased expression of genes involved in auxin, expansin, and gibberellin biosynthesis and metabolism in plant leaves exposed to the two volatile blends, while cytokinin and ethylene expression levels were decreased or similar in comparison with the control. These findings demonstrate that naturally occurring fungal VOCs can induce plant growth promotion and provide new insights into the mechanism of PGP activity. The application of stimulatory volatiles for growth enhancement could be used in the agricultural industry to increase crop yield.

Computational Interaction Analysis of Sirex noctilio Odorant-Binding Protein (SnocOBP7) Combined with Female Sex Pheromones and Symbiotic Fungal Volatiles

Sirex noctilio, a major forestry quarantine pest, has spread rapidly and caused serious harm. However, existing methods still need to be improved because its olfactory interaction mechanisms are poorly understood. In order to study the role of male-specific protein SnocOBP7 in the protein–ligand interactions, we selected it as the object of computational simulation and analysis. By docking it with 11 ligands and evaluating free binding energy decomposition, the three best binding ligands were found to be female sex pheromones ((Z)-7-heptacosene and (Z)-7-nonacosene) and symbiotic fungal volatiles ((−)-globulol). Binding mode analysis and computational alanine scanning suggested that five residues play key roles in the binding of each female sex pheromone to SnocOBP7, whereas two residues play key roles in (−)-globulol binding. Phe108 and Leu36 may be the crucial sites via which SnocOBP7 binds female sex pheromones, whereas Met40 may regulate the courtship behavior of males, and Leu61 may be related to mating and host finding. Our studies predicted the function of SnocOBP7 and found that the interaction between SnocOBP7 and pheromone is a complex process, and we successfully predicted its binding key amino-acid sites, providing a basis for the development of new prevention and control methods relying on female sex pheromones and symbiotic fungi.

A double-edged sword: Amylostereum areolatum odors attract both Sirex noctilio (Hymenoptera: Siricidae) and its parasitoid, Ibalia leucospoides

The Eurasian woodwasp, Sirex noctilio, is an invasive pest of pines in temperate regions of the Southern Hemisphere, and has been introduced to North America. A parasitoid, Ibalia leucospoides, has been broadly employed for biological control of this pest. Volatiles emitted from the fungal symbiont of S. noctilio, Amylostereum areolatum, are reliable cues for S. noctilio and I. leucospoides females to optimize their foraging behavior (host location and host habitat finding) in a chemically complex environment. The headspace volatiles of A. areolatum, were analyzed using coupled gas chromatography-mass spectrometry (GC-MS) and GC-electroantennographic detection (GC-EAD) for both S. noctilio and I. leucospoides females. Analyses revealed that both species could detect several fungal volatiles. In olfactometer bioassays, S. noctilio females were attracted to a 4-component blend of 6-methyl-5-hepten-2-one, trans-3-hexenyl acetate, linalool, and geraniol, while the addition of ρ-anisaldehyde to the blend was necessary for attraction of I. leucospoides females. The results of trap catches in field experiments confirmed that these fungal volatiles in combination with host tree volatiles are attractive to both species, although the release rate of the fungal volatiles is important. These volatiles can serve as a basis for the development of improved lures for both species.

Eight-carbon volatiles: prominent fungal and plant interaction compounds.

Signaling via volatile organic compounds (VOCs) has historically been studied mostly by entomologists; however, botanists and mycologists are increasingly aware of the physiological potential of chemical communication in the gas phase. Most research to date focuses on the observed effects of VOCs on different organisms such as differential growth or metabolite production. However, with the increased interest in volatile signaling, more researchers are investigating the molecular mechanisms for these effects. Eight-carbon VOCs are among the most prevalent and best-studied fungal volatiles. Therefore, this review emphasizes examples of eight-carbon VOCs affecting plants and fungi. These compounds display different effects that include growth suppression in both plants and fungi, induction of defensive behaviors such as accumulation of mycotoxins, phytohormone signaling cascades, and the inhibition of spore and seed germination. Application of '-omics' and other next-generation sequencing techniques is poised to decipher the mechanistic basis of volatiles in plant-fungal communication.

Volatile emission and biosynthesis in endophytic fungi colonizing black poplar leaves.

Plant volatiles play a major role in plant–insect interactions as defense compounds or attractants for insect herbivores. Recent studies have shown that endophytic fungi are also able to produce volatiles and this raises the question of whether these fungal volatiles influence plant–insect interactions. Here, we qualitatively investigated the volatiles released from 13 endophytic fungal species isolated from leaves of mature black poplar (Populus nigra) trees. The volatile blends of these endophytes grown on agar medium consist of typical fungal compounds, including aliphatic alcohols, ketones and esters, the aromatic alcohol 2-phenylethanol and various sesquiterpenes. Some of the compounds were previously reported as constituents of the poplar volatile blend. For one endophyte, a species of Cladosporium, we isolated and characterized two sesquiterpene synthases that can produce a number of mono- and sesquiterpenes like (E)-β-ocimene and (E)-β-caryophyllene, compounds that are dominant components of the herbivore-induced volatile bouquet of black poplar trees. As several of the fungus-derived volatiles like 2-phenylethanol, 3-methyl-1-butanol and the sesquiterpene (E)-β-caryophyllene, are known to play a role in direct and indirect plant defense, the emission of volatiles from endophytic microbial species should be considered in future studies investigating tree-insect interactions.

Transcriptome of different fruiting stages in the cultivated mushroom Cyclocybe aegerita suggests a complex regulation of fruiting and reveals enzymes putatively involved in fungal oxylipin biosynthesis

BackgroundCyclocybe aegerita (syn. Agrocybe aegerita) is a commercially cultivated mushroom. Its archetypal agaric morphology and its ability to undergo its whole life cycle under laboratory conditions makes this fungus a well-suited model for studying fruiting body (basidiome, basidiocarp) development. To elucidate the so far barely understood biosynthesis of fungal volatiles, alterations in the transcriptome during different developmental stages of C. aegerita were analyzed and combined with changes in the volatile profile during its different fruiting stages.ResultsA transcriptomic study at seven points in time during fruiting body development of C. aegerita with seven mycelial and five fruiting body stages was conducted. Differential gene expression was observed for genes involved in fungal fruiting body formation showing interesting transcriptional patterns and correlations of these fruiting-related genes with the developmental stages. Combining transcriptome and volatilome data, enzymes putatively involved in the biosynthesis of C8 oxylipins in C. aegerita including lipoxygenases (LOXs), dioxygenases (DOXs), hydroperoxide lyases (HPLs), alcohol dehydrogenases (ADHs) and ene-reductases could be identified. Furthermore, we were able to localize the mycelium as the main source for sesquiterpenes predominant during sporulation in the headspace of C. aegerita cultures. In contrast, changes in the C8 profile detected in late stages of development are probably due to the activity of enzymes located in the fruiting bodies.ConclusionsIn this study, the combination of volatilome and transcriptome data of C. aegerita revealed interesting candidates both for functional genetics-based analysis of fruiting-related genes and for prospective enzyme characterization studies to further elucidate the so far barely understood biosynthesis of fungal C8 oxylipins.

Electrophysiological and Behavioral Responses of an Ambrosia Beetle to Volatiles of its Nutritional Fungal Symbiont

Ambrosia beetles (Coleoptera: Scolytinae) cultivate their fungal symbiont within host substrates as the sole source of nutrition on which the larvae and adults must feed. To investigate a possible role for semiochemicals in this interaction, we characterized electrophysiological and behavioral responses of Xylosandrus germanus to volatiles associated with its fungal symbiont Ambrosiella grosmanniae. During still-air walking bioassays, X. germanus exhibited an arrestment response to volatiles of A. grosmanniae, but not antagonistic fungi Beauveria bassiana, Metarhizium brunneum, Trichoderma harzianum, the plant pathogen Fusarium proliferatum, or malt extract agar. Solid phase microextraction-gas chromatography-mass spectrometry identified 2-ethyl-1-hexanol, 2-phenylethanol, methyl benzoate and 3-methyl-1-butanol in emissions from A. grosmanniae; the latter two compounds were also detected in emissions from B. bassiana. Concentration-responses using electroantennography documented weak depolarizations to A. grosmanniae fungal volatiles, unlike the comparatively strong response to ethanol. When tested singly in walking bioassays, volatiles identified from A. grosmanniae elicited relatively weak arrestment responses, unlike the responses to ethanol. Xylosandrus germanus also exhibited weak or no long-range attraction to the fungal volatiles when tested singly during field trials in 2016–2018. None of the fungal volatiles enhanced attraction of X. germanus to ethanol when tested singly; in contrast, 2-phenylethanol and 3-methyl-1-butanol consistently reduced attraction to ethanol. Volatiles emitted by A. grosmanniae may represent short-range olfactory cues that could aid in distinguishing their nutritional fungal symbiont from other fungi, but these compounds are not likely to be useful as long-range attractants for improving detection or mass trapping tactics.

Proteostatic Regulation of MEP and Shikimate Pathways by Redox-Activated Photosynthesis Signaling in Plants Exposed to Small Fungal Volatiles.

Microorganisms produce volatile compounds (VCs) with molecular masses of less than 300 Da that promote plant growth and photosynthesis. Recently, we have shown that small VCs of less than 45 Da other than CO2 are major determinants of plant responses to fungal volatile emissions. However, the regulatory mechanisms involved in the plants’ responses to small microbial VCs remain unclear. In Arabidopsis thaliana plants exposed to small fungal VCs, growth promotion is accompanied by reduction of the thiol redox of Calvin-Benson cycle (CBC) enzymes and changes in the levels of shikimate and 2-C-methyl-D-erythritol 4-phosphate (MEP) pathway-related compounds. We hypothesized that plants’ responses to small microbial VCs involve post-translational modulation of enzymes of the MEP and shikimate pathways via mechanisms involving redox-activated photosynthesis signaling. To test this hypothesis, we compared the responses of wild-type (WT) plants and a cfbp1 mutant defective in a redox-regulated isoform of the CBC enzyme fructose-1,6-bisphosphatase to small VCs emitted by the fungal phytopathogen Alternaria alternata. Fungal VC-promoted growth and photosynthesis, as well as metabolic and proteomic changes, were substantially weaker in cfbp1 plants than in WT plants. In WT plants, but not in cfbp1 plants, small fungal VCs reduced the levels of both transcripts and proteins of the stromal Clp protease system and enhanced those of plastidial chaperonins and co-chaperonins. Consistently, small fungal VCs promoted the accumulation of putative Clp protease clients including MEP and shikimate pathway enzymes. clpr1-2 and clpc1 mutants with disrupted plastidial protein homeostasis responded weakly to small fungal VCs, strongly indicating that plant responses to microbial volatile emissions require a finely regulated plastidial protein quality control system. Our findings provide strong evidence that plant responses to fungal VCs involve chloroplast-to-nucleus retrograde signaling of redox-activated photosynthesis leading to proteostatic regulation of the MEP and shikimate pathways.

Trichoderma atroviride‐emitted volatiles improve growth of Arabidopsis seedlings through modulation of sucrose transport and metabolism

Plants host a diverse microbiome and differentially react to the fungal species living as endophytes or around their roots through emission of volatiles. Here, using divided Petri plates for Arabidopsis-T. atroviride co-cultivation, we show that fungal volatiles increase endogenous sugar levels in shoots, roots and root exudates, which improve Arabidopsis root growth and branching and strengthen the symbiosis. Tissue-specific expression of three sucrose phosphate synthase-encoding genes (AtSPS1F, AtSPS2F and AtSPS3F), and AtSUC2 and SWEET transporters revealed that the gene expression signatures differ from those of the fungal pathogens Fusarium oxysporum and Alternaria alternata and that AtSUC2 is largely repressed either by increasing carbon availability or by perception of the fungal volatile 6-pentyl-2H-pyran-2-one. Our data point to Trichoderma volatiles as chemical signatures for sugar biosynthesis and exudation and unveil specific modulation of a critical, long-distance sucrose transporter in the plant.

Belowground fungal volatiles perception in okra (Abelmoschus esculentus) facilitates plant growth under biotic stress

Microbial volatile organic compounds (mVOCs) have great potential in plant ecophysiology, yet the role of belowground VOCs in plant stress management remains largely obscure. Analysis of biocontrol producing VOCs into the soil allow detailed insight into their interaction with soil borne pathogens for plant disease management. A root interaction trial was set up to evaluate the effects of VOCs released from Trichoderma viride BHU-V2 on soil-inhabiting fungal pathogen and okra plant growth. VOCs released into soil by T. viride BHU-V2 inhibited the growth of collar rot pathogen, Sclerotium rolfsii. Okra plants responded to VOCs by increasing the root growth (lateral roots) and total biomass content. VOCs exposure increased defense mechanism in okra plants by inducing different enzyme activities i.e. chitinase (0.89 fold), β-1,3-glucanase (0.42 fold), peroxidase (0.29 fold), polyphenol oxidase (0.33 fold) and phenylalanine lyase (0.7 fold) when inoculated with S. rolfsii. In addition, T. viride BHU-V2 secreted VOCs reduced lipid peroxidation and cell death in okra plants under pathogen inoculated condition. GC/MS analysis of VOCs blend revealed that T. viride BHU-V2 produced more number of antifungal compounds in soil medium as compared to standard medium. Based on the above observations it is concluded that okra plant roots perceive VOCs secreted by T. viride BHU-V2 into soil that involved in induction of plant defense system against S. rolfsii. In an ecological context, the findings reveal that belowground microbial VOCs may play an important role in stress signaling mechanism to interact with plants.

Fungal volatiles emitted by members of the microbiome of desert plants are diverse and capable of promoting plant growth.

Fungi represent a group of eukaryotic microorganisms that are an important part of the plant microbiome. They produce a vast array of metabolites, including fungal volatile organic compounds (fVOCs). However, the diversity and biological activities of fVOCs emitted by the mycobiota of plants native to arid and semi-arid environments remain under-explored. We characterized the chemical diversity of fVOCs produced by 22 representative members of the microbiome of agaves and cacti using SPME-GC-MS. We further tested the effects of pure compounds on the growth and development of Arabidopsis thaliana and host plants. Members of the Sordariomycetes (nine strains), Eurotiomycetes (three), Dothideomycetes (eight), Saccharomycetes (one) and Mucoromycetes (one) were included in our study. We identified 94 fungal organic volatiles classified into nine chemical classes. Terpenes showed the greatest chemical diversity, followed by alcohols and aliphatic compounds. We discovered that camphene and benzyl benzoate, together with the widely distributed and already tested benzyl alcohol, 2-phenylethyl alcohol and 3-methyl-1-butanol, improved plant growth and development of A. thaliana, Agave tequilana and Agave salmiana. Our studies on the fungal VOCs from desert plants underscore an untapped chemical diversity with promising biotechnological applications.

Function of sesquiterpenes from Schizophyllum commune in interspecific interactions.

Wood is a habitat for a variety of organisms, including saprophytic fungi and bacteria, playing an important role in wood decomposition. Wood inhabiting fungi release a diversity of volatiles used as signaling compounds to attract or repel other organisms. Here, we show that volatiles of Schizophyllum commune are active against wood-decay fungi and bacteria found in its mycosphere. We identified sesquiterpenes as the biologically active compounds, that inhibit fungal growth and modify bacterial motility. The low number of cultivable wood inhabiting bacteria prompted us to analyze the microbial community in the mycosphere of S. commune using a culture-independent approach. Most bacteria belong to Actinobacteria and Proteobacteria, including Pseudomonadaceae, Sphingomonadaceae, Erwiniaceae, Yersiniaceae and Mariprofundacea as the dominating families. In the fungal community, the phyla of ascomycetes and basidiomycetes were well represented. We propose that fungal volatiles might have an important function in the wood mycosphere and could meditate interactions between microorganisms across domains and within the fungal kingdom.

Volatiles from the fungus Fusarium oxysporum affect interactions of Brassica rapa plants with root herbivores

1. Soil is a diverse and heterogeneous environment where chemicals mediate numerous interactions between soil organisms and plants. To date, studies have extensively addressed volatile‐mediated interactions between soil microorganisms and the effects of microbial volatiles on plant growth. Yet, to our knowledge, it remains to be explored whether volatiles from soil‐borne fungi can influence plant interactions with root herbivores, facilitating or hampering performance of competitors that share the same host plant.2. In the present study, we investigated the effects of volatiles emitted by the soil‐borne fungus Fusarium oxysporum on the performance of two root herbivores: the plant parasitic cyst nematode, Heterodera schachtii, and the insect root herbivore, Delia radicum, upon infestation of Brassica rapa roots.3. Fungal volatiles slowed down the development of the root nematode cysts but increased their size, suggesting an enhanced egg load. In contrast, the performance of the insect root herbivore was unaffected by the exposure of roots to fungal volatiles. Additionally, fungal volatiles promoted the growth of plants infested with the root nematode, but not of those infested with the insect root herbivore.4. Together, our data show that volatiles from a soil‐borne fungus can affect root interactions with root herbivores. Increased production of nematode eggs and plant growth promotion suggest a specific modulation of root‐herbivore interactions by fungal volatiles.

Fungal Volatiles as Olfactory Cues for Female Fungus Gnat, Lycoriella ingenua in the Avoidance of\xa0Mycelia Colonized Compost

The chemical signatures emitted by fungal substrates are key components for mycophagous insects in the search for food source or for suitable oviposition sites. These volatiles are usually emitted by the fruiting bodies and mycelia. The volatiles attract fungivorous insects, like flowers attract pollinators; certain flowers mimic the shape of mushroom fruiting bodies and even produce a typical mushroom odor to exploit on fungus-insect mutualism. There are numerous insects which are mycophagous or eat fungi additionally, but only a few are considered a threat in agriculture. Lycoriella ingenua is one of the most serious pests in mushroom cultivation worldwide. Here we attempt to examine the role of environmental volatiles upon behavioral oviposition preference. In two-choice bioassays, fungus gnats preferred uncolonized compost compared to colonized compost but preferred colonized compost against nothing. However, when colonized compost was paired against distilled water, no significant choice was observed. The comparison of fresh casing material and mycelium colonized casing material resulted in no significant preference. From colonized compost headspace, three antennally active volatiles were isolated by gas chromatography coupled with electroantennography and subsequently identified with gas chromatography coupled mass spectrometry as 1-hepten-3-ol, 3-octanone and 1-octen-3-ol. In behavioral assays the addition of said synthetic volatiles to uncolonized compost separately and in combination to mimic colonized compost resulted in avoidance. We thus partially elucidate the role of fungal volatiles in the habitat seeking behavior of Lycoriella ingenua.

Volatiles from soil‐borne fungi affect directional growth of roots

Volatiles play major roles in mediating ecological interactions between soil (micro)organisms and plants. It is well‐established that microbial volatiles can increase root biomass and lateral root formation. To date, however, it is unknown whether microbial volatiles can affect directional root growth. Here, we present a novel method to study belowground volatile‐mediated interactions. As proof‐of‐concept, we designed a root Y‐tube olfactometer, and tested the effects of volatiles from four different soil‐borne fungi on directional growth of Brassica rapa roots in soil. Subsequently, we compared the fungal volatile organic compounds (VOCs) previously profiled with Gas Chromatography–Mass Spectrometry (GC–MS). Using our newly designed setup, we show that directional root growth in soil is differentially affected by fungal volatiles. Roots grew more frequently toward volatiles from the root pathogen Rhizoctonia solani, whereas volatiles from the other three saprophytic fungi did not impact directional root growth. GC–MS profiling showed that six VOCs were exclusively emitted by R. solani. These findings verify that this novel method is suitable to unravel the intriguing chemical cross‐talk between roots and soil‐borne fungi and its impact on root growth.

Fungal volatiles influence plant defence against above‐ground and below‐ground herbivory

Abstract Plants have evolved resistance traits that negatively affect attackers, and tolerance traits that sustain plant growth despite herbivore damage. These mechanisms often co‐occur in a mixed‐defence strategy, balancing resistance and tolerance. These plant defences can be enhanced upon interaction with soil micro‐organisms. Here we investigated the effects of volatiles emitted by soil‐borne fungi on plant defence to insect herbivory, and on plant phenology. We exposed roots of Brassica rapa plants to volatiles emitted by four soil‐borne fungi. As a proxy of plant resistance, we assessed the performance of Pieris brassicae, a caterpillar feeding on leaves and inflorescences, and of Delia radicum, an insect root herbivore. As a proxy of plant tolerance, we compared growth of volatile‐exposed plants challenged with or without insects. Additionally, we assessed the effects on plant phenology by recording bolting time and by counting the number of buds and flowers. Plant exposure to fungal volatiles differentially affected plant resistance to above‐ and below‐ground herbivory. Performance of P. brassicae caterpillars differed between the fungal volatile‐exposed plants but was variable between experimental batches. In contrast, the effects of fungal volatiles on D. radicum performance were predominantly negative, indicating an increased plant resistance. Despite root consumption by D. radicum, root dry weight remained unchanged in infested plants compared with uninfested ones, irrespectively of the volatile exposure, suggesting compensation for the tissue loss, sometimes at the cost of undamaged above‐ground tissues. When B. rapa plants were attacked by P. brassicae caterpillars, only exposure to volatiles of some fungi led to compensation for the loss of above‐ground tissues consumed by the caterpillars, which differed between leaves and inflorescences. Furthermore, bolting was accelerated in response to volatiles of some fungi, resulting in more buds and flowers, which suggests a potential enhancement of plant fitness. Our data show that fungal volatiles can modulate the mixed‐defence strategies of B. rapa plants, balancing plant resistance and tolerance to above‐ and below‐ground herbivory. These effects may be variable and were fungus specific. Ultimately, plant fitness may be enhanced upon root exposure to fungal volatiles. A free Plain Language Summary can be found within the Supporting Information of this article.

Fungal volatiles mediate cheese rind microbiome assembly

In vitro studies in plant, soil, and human systems have shown that microbial volatiles can mediate microbe-microbe or microbe-host interactions. These previous studies have often used artificially high concentrations of volatiles compared to in situ systems and have not demonstrated the roles volatiles play in mediating community-level dynamics. We used the notoriously volatile cheese rind microbiome to identify bacteria responsive to volatiles produced by five widespread cheese fungi. Vibrio casei had the strongest growth stimulation when exposed to all fungi. In multispecies community experiments, fungal volatiles caused a shift to a Vibrio-dominated community, potentially explaining the widespread occurrence of Vibrio in surface-ripened cheeses. RNA sequencing identified activation of the glyoxylate shunt as a possible mechanism underlying volatile-mediated growth promotion and community assembly. Our study demonstrates how airborne chemicals could be used to control the composition of microbiomes and illustrates how volatiles may impact the development of cheese rinds.

Exposure to Fungal Volatiles Can Influence Volatile Emissions From Other Ophiostomatoid Fungi.

Fungal volatile organic compounds (FVOCs) can act as intra- and inter-kingdom communication signals that influence the growth and behaviors of organisms involved in antagonistic or mutualistic relationships with fungi. There is growing evidence suggesting that FVOCs can mediate interactions between organisms within and across different ecological niches. Bark beetles have established mutualistic relationships with ophiostomatoid fungi which can serve as a food source and condition host plant tissues for developing beetle larvae. While the profiles (both composition and concentrations) of volatile emission from ophiostomatoid fungi can be influenced by abiotic factors, whether emissions from a given fungal species can be influenced by those from another is still unknown. Here, we analyzed FVOCs emitted from the two ophiostomatoid fungi, Grosmannia clavigera and Ophiostoma ips, associated with mountain pine beetle and pine engraver beetle, respectively, when each fungus was growing alone or in a shared headspace. We used two isolates of each fungus species. Overall, we detected a total of eight volatiles in both G. clavigera alone or in combination with O. ips including acetoin, ethyl acetate, cis-grandisol, isoamyl alcohol, isobutanol, 2-methyl-1-butanol, phenethyl acetate, and phenethyl alcohol. The profiles of volatiles emitted differed between the two fungal species but not between the two isolates of the same fungus. Six compounds were common between the species, whereas two compounds were detected only when G. clavigera was present. Moreover, the majority of volatiles were detected less frequently and at lower concentrations when the two fungi were grown together in a shared headspace. These results are likely due to reduced volatile emissions from O. ips in the presence of G. clavigera. However, changes in the profiles of fungal volatiles did not correspond with the observed changes in the growth of either species. Overall, these results suggest that the similarities in fungal volatiles among different species of fungi may reflect a common ecological niche and that the differences may correspond to species-specific adaptation to their respective host beetles or genetic factors.