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Abstract Microbial volatile organic compounds may act as semiochemicals, inciting different behavioral responses in insects. Beauveria bassiana is an entomopathogenic fungus, and physiological and environmental factors are positively related to fungal virulence. In this study, we examined the volatile profiles produced by eight B. bassiana strains, isolated from soil plots and mycosed insect cadavers, with different speeds of kill and determined if these compounds induce oviposition behavior in Spodoptera frugiperda. Fungal volatilome analysis revealed differences between the isolates. Isolates from mycosed insects showed higher virulence, larger egg mass area and length, and a higher number of eggs by mass, than those obtained from soil. Furthermore, a dilution of the fungal odoriferous compounds increased the insect response, suggesting that S. frugiperda is highly susceptible to the fungal compound’s fingerprint. Otherwise, the insect response to the natural blend of volatiles released by the fungus was different from that obtained with 3-methylbutanol, which was the most abundant compound in all isolates. The ability of an entomopathogen to produce volatiles that can induce olfactory stimulation of egg-laying behavior could represent an ecological adaptive advantage in which the entomopathogen stimulates the insect population growth. The pool of volatiles released by B. bassiana was specific to the isolate source from which the fungus was obtained and S. frugiperda responded according to the fungal compounds fingerprint.

All odorants are volatile organic compounds (VOCs), i.e., low molecular weight compounds that easily evaporate at normal temperatures and pressure. Fungal VOCs are relatively understudied compared to VOCs of bacterial, plant, or synthetic origin. Much of the research to date on fungal VOCs has focused on their food and flavor properties, their use as indirect indicators of fungal growth in agriculture, or their role as semiochemicals for insects. In addition, research into fungal volatiles has also taken place to monitor spoilage, for purposes of chemotaxonomy, for use in biofilters and for biodiesel, to detect plant and animal disease, for “mycofumigation,” and with respect to plant health. As methods for the analysis of gas phase molecules have improved, it has become apparent that fungal VOC are more chemically varied and more biologically active than has generally been realized. In particular, there is increasing data that show that fungal VOCs frequently mediate interactions between organisms within and across different ecological niches. The goal of this mini review is to orchestrate data on fungal VOCs obtained from disparate disciplines as well as to draw attention to the ecological importance of fungal VOCs in signaling between different species. Technologies and approaches that are common in one area of research are often unknown in others, and the study of fungal VOCs would benefit from more cross talk between subdisciplines.

Microbial volatile organic compounds (MVOCs) are mixtures of gas-phase hydrophobic carbon-based molecules produced by microorganisms such as bacteria and fungi. They can act as airborne signals sensed by plants being crucial players in triggering signaling cascades influencing their secondary metabolism, development, and growth. The role of fungal volatile organic compounds (FVOCs) from beneficial or detrimental species to influence the physiology and priming effect of plants has been well studied. However, the plants mechanisms to discern between FVOCs from friend or foe remains significantly understudied. Under this outlook, we present an overview of the VOCs produced by plant-associate fungal species, with a particular focus on the challenges faced in VOCs research: i ) understanding how plants could perceive FVOCs, ii ) investigating the differential responses of plants to VOCs from beneficial or detrimental fungal strains, and finally, iii ) exploring practical aspects related to the collection of VOCs and their eco-friendly application in agriculture.

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.

Many plant and fungal species use volatile organic compounds (VOCs) as chemical signals to convey information about the location or quality of their fruits or fruiting bodies to animal dispersers. Identifying the environmental factors and biotic interactions that shape fruit selection by animals is key to understanding the evolutionary processes that underpin chemical signaling. Using four Elaphomyces truffle species, we explored the role of fruiting depth, VOC emissions, and protein content in selection by five rodent species. We used stable isotope analysis of nitrogen (δ15N) in truffles to estimate fruiting depth, proton-transfer-reaction mass spectrometry to determine volatile emission composition, and nitrogen concentrations to calculate digestible protein of truffles. We coupled field surveys of truffle availability with truffle spore loads in rodent scat to determine selection by rodents. Despite presumably easier access to the shallow fruiting species, E. americanus (0.5-cm depth) and E. verruculosus (2.5-cm depth), most rodents selected for truffles fruiting deeper in the soil, E. macrosporus (4.1-cm depth) and E. bartlettii (5.0-cm depth). The deeper fruiting species had distinct VOC profiles and produced significantly higher quantities of odiferous compounds. Myodes gapperi (southern red-backed vole), a fungal specialist, also selected for truffles with high levels of digestible protein, E. verruculosus and E. macrosporus. Our results highlight the importance of chemical signals in truffle selection by rodents and suggest that VOCs are under strong selective pressures relative to protein rewards. Strong chemical signals likely allow detection of truffles deep within the soil and reduce foraging effort by rodents. Finally, for rodents that depend on fungi as a major food source, protein content may also be important in selecting truffles.

Beneficial soil microorganisms can affect plant growth and resistance by the production of volatile organic compounds (VOCs). Yet, little is known on how VOCs from soil-borne plant pathogens affect plant growth and resistance. Here we show that VOCs released from mycelium and sclerotia of the fungal root pathogen enhance growth and accelerate development of . Seedlings briefly exposed to the fungal VOCs showed similar phenotypes, suggesting that enhanced biomass and accelerated development are primed already at early developmental stages. Fungal VOCs did not affect plant resistance to infection by the VOC-producing pathogen itself but reduced aboveground resistance to the herbivore . Transcriptomics of revealed that genes involved in auxin signaling were up-regulated, whereas ethylene and jasmonic acid signaling pathways were down-regulated by fungal VOCs. Mutants disrupted in these pathways showed similar VOC-mediated growth responses as the wild-type , suggesting that other yet unknown pathways play a more prominent role. We postulate that uses VOCs to predispose plants for infection from a distance by altering root architecture and enhancing root biomass. Alternatively, plants may use enhanced root growth upon fungal VOC perception to sacrifice part of the root biomass and accelerate development and reproduction to survive infection.

Many plant and fungal species use volatile organic compounds (VOCs) as chemical signals to convey information about the location or quality of their fruits or fruiting bodies to animal dispersers. Identifying the environmental factors and biotic interactions that shape fruit selection by animals is key to understanding the evolutionary processes that underpin chemical signaling. Using four Elaphomyces truffle species, we explored the role of fruiting depth, VOC emissions, and protein content in selection by five rodent species. We used stable isotope analysis of nitrogen (δ15N) in truffles to estimate fruiting depth, proton-transfer-reaction mass spectrometry to determine volatile emission composition, and nitrogen concentrations to calculate digestible protein of truffles. We coupled field surveys of truffle availability with truffle spore loads in rodent scat to determine selection by rodents. Despite presumably easier access to the shallow fruiting species, E. americanus (0.5-cm depth) and E. verruculosus (2.5-cm depth), most rodents selected for truffles fruiting deeper in the soil, E. macrosporus (4.1-cm depth) and E. bartlettii (5.0-cm depth). The deeper fruiting species had distinct VOC profiles and produced significantly higher quantities of odiferous compounds. Myodes gapperi (southern red-backed vole), a fungal specialist, also selected for truffles with high levels of digestible protein, E. verruculosus and E. macrosporus. Our results highlight the importance of chemical signals in truffle selection by rodents and suggest that VOCs are under strong selective pressures relative to protein rewards. Strong chemical signals likely allow detection of truffles deep within the soil and reduce foraging effort by rodents. For rodents that depend on fungi as a major food source, protein content may also be important in selecting truffles.

The diel flight activity in Cathartus quadricollis (Guerin-Meneville) (Coleoptera: Silvanidae), a predator of two important pests in Hawaii, coffee berry borer, Hypothenemus hampei (Ferrari) and tropical nut borer, Hypothenemus obscurus (F.) (Coleoptera: Curculionidae: Scolytinae) was studied in a macadamia nut orchard using yellow sticky traps baited with pheromone and fungal volatile attractants. The study was conducted at different months throughout the year and at different times during the lunar cycle (new moon and full moon). Flight activity peaked in the late hours of the photophase into the early hours of the scotophase, between 1830 and 2000 h; flight activity also occurred but to a lesser extent in the early morning hours between 0700 and 1030 h. Numbers of captured C. quadricollis during periods of flight activity were negatively correlated with wind speed. The implications of these findings for the development of optimal pest management strategies including biological control are discussed.

Rhizospheric microorganisms can alter plant physiology and morphology in many different ways including through the emission of volatile organic compounds (VOCs). Here we demonstrate that VOCs from beneficial root endophytic Serendipita spp. are able to improve the performance of in vitro grown Arabidopsis seedlings, with an up to 9.3-fold increase in plant biomass. Additional changes in VOC-exposed plants comprised petiole elongation, epidermal cell and leaf area expansion, extension of the lateral root system, enhanced maximum quantum efficiency of photosystem II (Fv/Fm), and accumulation of high levels of anthocyanin. Notwithstanding that the magnitude of the effects was highly dependent on the test system and cultivation medium, the volatile blends of each of the examined strains, including the references S. indica and S. williamsii , exhibited comparable plant growth-promoting activities. By combining different approaches, we provide strong evidence that not only fungal respiratory CO2 accumulating in the headspace, but also other volatile compounds contribute to the observed plant responses. Volatile profiling identified methyl benzoate as the most abundant fungal VOC, released especially by Serendipita cultures that elicit plant growth promotion. However, under our experimental conditions, application of methyl benzoate as a sole volatile did not affect plant performance, suggesting that other compounds are involved or that the mixture of VOCs, rather than single molecules, accounts for the strong plant responses. Using Arabidopsis mutant and reporter lines in some of the major plant hormone signal transduction pathways further revealed the involvement of auxin and cytokinin signaling in Serendipita VOC-induced plant growth modulation. Although we are still far from translating the current knowledge into the implementation of Serendipita VOCs as biofertilizers and phytostimulants, volatile production is a novel mechanism by which sebacinoid fungi can trigger and control biological processes in plants, which might offer opportunities to address agricultural and environmental problems in the future.

Many endophytic fungi are approved as plant growth stimulants, and several commercial biostimulants have already been introduced in agricultural practice. However, there are still many species of fungi whose plant growth-promoting properties have been understudied or not studied at all. We examined the growth-promoting effect in spring barley (Hordeum vulgare) and Italian ryegrass (Lolium multiflorum) induced by three endophytic fungi previously obtained from the roots of Festuca/Lolium grasses. Surface-sterilized seeds were inoculated with a spore suspension of Cadophora fastigiata (isolate BSG003), Paraphoma fimeti (BSG010), Plectosphaerella cucumerina (BSG006), and their spore mixture. Before harvesting, the inoculated plants were grown in a greenhouse, with the barley being in multi-cavity trays for 30 days and ryegrass being placed in an original cylindric element system for 63 days. All three newly tested fungi had a positive effect on the growth of the barley and ryegrass plants, with the most pronounced impact observed in their root size. The fungal inoculations increased the dry shoot biomass between 11% and 26% in Italian ryegrass, but no such impact was observed in barley. The highest root increment was observed in barley. Herein, P. cucumerina and C. fastigiata inoculations were superior to other treatments, showing an increase in root dry weight of 50% compared to 20%, respectively. All fungal inoculations significantly promoted root growth in Italian ryegrass, resulting in a 20–30% increase in dry weight compared to non-inoculated plants. Moreover, a strong stimulatory effect of the fungi-emitted VOCs on the root development was observed in plate-in-plate arrays. In the presence of C. fastigiata and P. cucumerina cultures, the number of roots and root hairs in barley seedlings doubled compared to control plants. Thus, in our study, we demonstrated the potential of the grass root-derived endophytes C. fastigiata, P. fimeti, and P. cucumerina as growth promoters for spring barley and Italian ryegrass. These studies can be extended to other major crops and grasses by evaluating different fungal isolates.