TY - JOUR
AU - Fani, Renato
AB - ABSTRACT Symbiosis involving two (or more) prokaryotic and/or eukaryotic partners is extremely widespread in nature, and it has performed, and is still performing, a key role in the evolution of several biological systems. The interaction between symbiotic partners is based on the emission and perception of a plethora of molecules, including volatile organic compounds (VOCs), synthesized by both prokaryotic and eukaryotic (micro)organisms. VOCs acquire increasing importance since they spread above and below ground and act as infochemicals regulating a very complex network. In this work we review what is known about the VOCs synthesized by fungi prior to and during the interaction(s) with their partners (either prokaryotic or eukaryotic) and their possible role(s) in establishing and maintaining the symbiosis. Lastly, we also describe the potential applications of fungal VOCs from different biotechnological perspectives, including medicinal, pharmaceutical and agronomical. volatilome, trans-kingdom communication, below-ground symbiosis, fungi, bacteria, plants, chemical ecology INTRODUCTION The purpose of this review is to draw attention to the volatile organic compounds (VOCs), which allow the formation and maintenance of mutualistic symbiotic relationships of fungi with plants and/or bacteria. The effect of fungal VOCs on the volatile production of different hosts and their ecological significance will be described. Furthermore, an overview of the biotechnological application of the VOCs involved in fungal symbioses will be provided. Communication is a crucial process for life. It starts from a sender releasing a message that has to be received and ‘understood’ by a receiver that can belong to any kingdom: inter-kingdom communication exists in both above- and below-ground environments and takes place between the aerial part of plants, associated microbes, insects and fungi on one side, and roots, soil microbiota and fungi on the other. These interactions are very complex, sophisticated, finely regulated and modulated, ranging from mutualistic to parasitic associations. The analysis of the information exchange between fungi and bacteria or plant cells has revealed the existence of an important inter- and intra-species communication (Tarkka, Sarniguet and Frey-Klett 2009). Fungi are highly sensitive organisms, perceiving themselves and distinguishing between ‘self’ and ‘not-self’. They are able to respond to environmental parameters and adapt their behavior in response to the fluctuations of either different external and/or internal stimuli. This per se implies that fungi exhibit signaling mediated communication processes not only between cells of the same organism, but also between different fungal species and organisms belonging to different domains (archaeae, bacteria and eucarya). Cell signaling networks both in intra- and inter-species communication (Feeney et al. 2006) have been suggested to be regulated by a complex and wide range of bioactive molecules synthesized as secondary metabolites by bacteria, invertebrates, fungi, lichens and plants. Thus, these organisms are thought to be the effectors of these associations modulating the biological processes in the soil ecosystem. VOLATILE ORGANIC COMPOUNDS The mixture of these bioactive molecules belongs to the general communicome, a term introduced in 2007 (Ray et al. 2007) to describe the whole set of proteomic factors involved in intercellular and organ communication in human medicine. If the bioactive molecules are bacterial VOCs this mix has been defined as volatilome (Maffei, Gertsch and Appendino 2011). The soil is a huge reservoir and source of biogenic volatile organic compounds, which are formed from decomposing litter and dead organic material or are synthesized by underground living organisms or organs and tissues of plants (Penuelas et al.2014). About 2000 volatiles from 1000 plant species (Dunkel et al. 2009), 1000 volatiles from 500 bacteria (hereinafter called bVOCs) (Lemfack et al. 2018) and about 300 volatiles from 70 fungi (hereinafter referred to as fVOCs) (Korpi, Jarnberg and Pasanen 2009; Lemfack et al. 2018) have been described up to now. Microbial and fungal volatiles are low molecular mass (<300 Da), odorous, carbon-based solid and liquid mixture compounds synthesized through different biosynthetic pathways and are emitted by bacteria, fungi, lichens, insects and plants. They belong to (at least) 48 chemical classes mainly represented by alkenes, alcohols, ketones and terpenoids (Kanchiswamy, Malnoy and Maffei 2015; Schmidt et al. 2015; Lemfack et al. 2018) that can vaporize and enter the gas phase at normal atmospheric temperature and pressure. They are lipophilic, are produced in the aqueous cellular phase and are released when the solution equilibrium is exceeded. Volatiles are emitted through diffusion or via passive or active transport (Effmert et al. 2006). Traditionally, VOCs produced by plants, fungi and bacteria are considered as just waste products; however, this scenario changed in the last decade when it was demonstrated that many of these molecules exhibit unexpected activities (Schmidt et al. 2015; Tyc et al. 2017). For instance, Groenhagen and coworkers (2013) demonstrated the correlation existing between bVOCs and acquired antibiotic resistance: indeed, the volatile blend emitted by Burkholderia ambifaria increases the Escherichia coli resistance to gentamicin and kanamycin. Also, the biogenic volatile compound trimethylamine, produced in animal tissues upon reduction of trimethylamine oxide, alters Gram-positive and Gram-negative human pathogen antibiotic resistance (Letoffe et al. 2014). Fungal volatiles Fungi not only release peptides, lipids and alcohols as soluble messengers into solution or onto solid media, they also synthesize a plethora of VOCs mainly belonging to alcohols, hydrocarbons, ketones, terpenes, alkanes and alkenes (Chiron and Michelot 2005). The qualitative and quantitative composition of the VOC's profile produced by a fungus depends on different physico-chemical parameters, such as temperature, oxygen and carbon source availability, pH and also on the age of the fungal culture (Blom et al. 2011; Thorn and Greenman 2012; Weise et al. 2012). Little is known about the biosynthesis and the physiological role of most fVOCs as well as their role as infochemicals. Many of them are the products of fatty acids breakdown catalyzed by lipoxygenases: 1-octen-3-ol and 10-oxo-acid are synthesized through the enzymatic oxidation and cleavage of linoleic and linolenic acids (Wurzenberger and Grosch 1984), whereas 3-methyl-1-butanol, 2-methyl-1-propanol and styrene arise from the metabolic transformation of some amino acids (Bjurman 1999), and dimethyl disulfide derives from methionine (Mason, Cortes and Horner 2010). Both the molecular structure and the pattern of fungal VOCs appear to be species or strain specific; for this reason, typical VOCs and their pattern can be used as a chemotaxonomic tool to identify fungal species either in single or mixed cultures. Fiedler, Schuetz and Geh (2001) have shown that some compounds, such as 1-octen-3-ol, 3-octanone, 2-methyl-1-butanol and 3-methyl-1-butanol (Fig. 1A), are present in many fungal species belonging to Trichoderma, Penicillium, Mucor, Fusarium and Aspergillus. Different strains belonging to the same species and different species of the same genus show a very similar and characteristic chromatographic pattern. For instance, three different isolates of Aspergillus versicolor produce 1,3 dimethoxy-benzene (Fischer et al. 1999; Fiedler, Schuetz and Geh 2001) and fungi belonging to this species can be easily identified by their characteristic sesquiterperpene fingerprint. Trans-β−caryophyllene is typical of Aspergillus fumigatus (Fischer et al. 1999), Trichoderma harzianum and Trichoderma pseudokoningii emit identical sesquiterpenes (Fiedler, Schuetz and Geh 2001), geosmin is a chemical marker for Penicillium expansum (Sonnichsen and Keller 1997), while dimethyl sulphide (Fig. 1A) is a good volatile indicator for both Stachybotrys chartarum and As. versicolor (Wessen et al. 2001). On the basis of different sesquiterpene patterns, ectomycorrhizal fungi can be distinguished between pathogenic and saprophytic ones (Muller et al. 2004). Figure 1. Open in new tabDownload slide Chemical structures of the volatile organic compounds that are the subject of this review and that are involved in fungal symbioses. Figure 1. Open in new tabDownload slide Chemical structures of the volatile organic compounds that are the subject of this review and that are involved in fungal symbioses. The fungal volatiles are important for self-recognition, defense processes and for inter-species recognition when hyphae of different fungi come into contact (Hynes et al. 2007). Fungal volatiles can also act as being fungistatic, suppressing soil disease by blocking the spores’ germination or affecting protein synthesis (Chuankun et al. 2004). Volatiles of soil-borne fungi benefit plants by activating defense responses and priming them against future pathogen attack (Hammerbacher et al. 2019). On the contrary, fVOCs can also negatively impact plant growth (Splivallo et al. 2007). Fungal volatiles can also have properties like pheromones (compounds that transmit signals between organisms of the same species), allomones (substances emitted by a member of one species that affect the behavior of another to the advantage of the emitter) and kairomones (compounds emitted by an individual of one species that benefit the recipient of a different species) (Mburu et al. 2011). fVOCs as quorum-sensing molecules Quorum sensing (QS), a phenomenon studied since 1960 in bacteria (Nealson, Platt and Hastings 1970), also takes place in fungi (Hornby 2001), where quorum-sensing molecules (both volatiles and non-volatiles) are involved in cross-kingdom communication (Dixon and Hall 2015). QS is involved in fungal morphogenesis, apoptosis, germination, pathogenicity and biofilm formation (Wongsuk, Pumeesat and Luplertlop 2016). In Candida albicans and Aspergillus spp., small molecules released from cells act as autoinducers and regulate the community depending on the cell population concentration (Padder, Prasad and Shah 2018). It has been shown that the pathogenic yeast C. albicans (Hogan 2006; Nickerson, Atkin and Hornby 2006) and the filamentous fungus Penicillium sclerotiorum (Raina, Odell and Keshavarz 2010) produce the volatile sesquiterpene farnesol (Fig. 1B) acting as a QS molecule. The volatile ammonia is transmitted by yeast colonies in pulses mediating an inter-colony signal (Palkova et al. 1997). Phenylethanol and tryptophol (Fig. 1B) induce pseudohyphal growth in Saccharomyces cerevisiae in a cell density-dependent way (Chen and Fink 2006). fVOCs and fungal lifestyle A correlation has been detected between filamentous fungi lifestyle and the type of VOCs produced. Saprophytic fungi live in the bulk and rhizospheric soil and feed on decaying organic matter that is available in their environment such as fallen trees, dead leaves, dead insects and animals. This group of fungi produce volatiles that maximize the nutrient availability around the hyphae by eliminating their competitors (Kottb et al. 2015), supporting plant growth (Lee et al. 2016) and enhancing plant immunity (Naznin et al. 2013). Endophytic fungi live within the plant tissue without showing any sign of harm (Rodriguez et al. 2009). Most known VOCs produced by endophytes have antimicrobial activity against filamentous fungal pathogens and oomycetes, while some also exhibit antibacterial properties (Gomes et al. 2018). Pathogenic fungi acquire nutrients from either feeding on living host cells or by killing them. Volatiles produced by these fungi show low chemical diversity and act as chemical stimuli to attract or repel interacting organisms. During interaction with host plants it seems that some fVOCs of pathogens work as a stimulant to enhance plant growth and accelerate its development (Cordovez et al. 2017). Foliar pathogens release VOCs that also improve the photosynthetic capacity of their plant host (Ameztoy et al. 2019). The fVOCs might predispose the hosts to pathogen infection by manipulating its cells to allocate energy and resources for growth rather than defense Mutualistic fungi also live on other living organisms, fungi obtain carbohydrates and protein from the host and in return they provide water and minerals that are not readily accessible to the host (Agrios 2005). The following sections examine the contribution provided by volatile molecules in fungal symbiosis with plants and bacteria. VOCS INVOLVEMENT IN FUNGAL SYMBIOSIS Symbiosis is the intimate association usually occurring between two organisms belonging to different species (Montoya, Pimm and Sole 2006). However, inter-specific below-ground microbial interactions often involve more than two (micro)organisms; this interaction may induce or suppress the production of VOCs with consequent alteration of VOCs profile composition (Piechulla, Lemfack and Kai 2017; Schulz-Bohm, Martín-Sánchez and Garbeva 2017). In the context of environmental ecology, mycorrhizae play a major role, due to their widespread presence and their importance in the nutrient cycle (Azcon-Aguilar and Barea 2015). In the sections below we consider the presence of volatile molecules both in arbuscular mychorrizae and ectomycorrhizae. VOCs in arbuscular mycorrhizae Mycorrhiza are different forms of symbiosis occurring with fungi of Glomales order and the roots of about 250 000 land plants species including gymnosperms, angiosperms and pteridophytes (Schussler and Kluge 2011). Mycorrhizae are split into ectomycorrhizae (EM) (Fig. 2D) and arbuscular mycorrhizae (AM) (Fig. 2A) depending on the infected area of the roots. The host plant (Fig. 2C) provides the endosymbiont with up to 20% of its photosynthetic products (Bago, Pfeffer and Shachar-Hill 2000) through a very efficient hyphal network connecting different plants (Simard 1997). The fungal hyphopodium enters the root giving rise to the arbuscle (Fig. 2A), the site where nutrients are exchanged. AM fungi develop extraradical hyphae several centimeters long into the soil (Auge 2001), interacting with other organisms and influencing the physiology of the plant root and its exudation pattern. During the establishment of the AM symbiosis, the root and the fungus communicate through exudates, small RNAs, reactive oxygen and nitrogen species, phytohormones, and also plant and fVOCs (Pineda 2013). In the pre-symbiotic phase (after spore germination) (Fig. 2B), the hyphal elongation and branching are elicited by plant flavonoids (Wang 2013; Gutjahr and Parniske 2013)). Bean and carrot roots produce unknown volatile attractants inducing the germination of AM fungus Gigaspora gigantea spores and their growth toward the host (Table 1) (Koske 1982) (Fig. 2A-C-1). On the other side, germinating spores of Gigaspora margarita produce still unknown volatiles that increase the number and the density of Lotus japonicus and Arabidopsis thaliana lateral roots (Table 1) (Fig. 2B-C-2) (Sun, Bonfante and Tang 2015), the preferred target for the AM colonization (Fusconi 2014). AM symbionts are also able to regulate host root orientation emitting sporal VOCs that modify the branch angle of the lateral roots, with a consequent increase in the chances of AM hyphae encountering plant roots in the rhizosphere (Table 1) (Fig. 2B-C-2) (Sun, Bonfante and Tang 2015). Since auxins regulate the branch angle of the lateral root, fVOCs can activate plant auxin signaling pathway (Roychoudhry et al. 2013). Figure 2. Open in new tabDownload slide Role of volatile molecules in orchestrating the different types of below-ground fungal symbioses. There is an important volatile exchange of information in the symbiosis between the spores (B) of arbuscular mycorrhizae (A) and the roots of the host plant (C): roots produce unknown volatile attractants (1) inducing the germination of AM fungus Gigaspora gigantea spores and their growth toward the host. Germinating spores of AM fungus produce still unknown volatiles (2) that increase the number and the density of host plant lateral roots. Ectomycorrhizae (D) and the roots of the host plant (E): aldehydes, ketones and alcohols are synthesized when Tuber borchii and the host plant Tilia americana interact in the pre-symbiotic stage to form an ectomycorrhizal. The origin of the VOCs is unclear (3–4). Symbiotic bacteria (F) of Tuber and Tuber fruiting body (G): fruiting bodies emit a complex mixture of almost 50 VOCs including methyl butanol, methyl propanol, phenylethanol and thiophene derivatives. The origin of the VOCs is unclear (5–6). Ectosymbiotic bacteria (H) of Fusarium oxysporum(I) and lettuce (L): β-caryophyllene (9) produced by F. oxysporum WT MSA35 (H + I) has a plant growth-promoting effect on lettuce (L); WT F. oxysporum (H + I) produces unknown VOCs (8) that inhibit the growth of phytopathogenic fungi (M). Figure 2. Open in new tabDownload slide Role of volatile molecules in orchestrating the different types of below-ground fungal symbioses. There is an important volatile exchange of information in the symbiosis between the spores (B) of arbuscular mycorrhizae (A) and the roots of the host plant (C): roots produce unknown volatile attractants (1) inducing the germination of AM fungus Gigaspora gigantea spores and their growth toward the host. Germinating spores of AM fungus produce still unknown volatiles (2) that increase the number and the density of host plant lateral roots. Ectomycorrhizae (D) and the roots of the host plant (E): aldehydes, ketones and alcohols are synthesized when Tuber borchii and the host plant Tilia americana interact in the pre-symbiotic stage to form an ectomycorrhizal. The origin of the VOCs is unclear (3–4). Symbiotic bacteria (F) of Tuber and Tuber fruiting body (G): fruiting bodies emit a complex mixture of almost 50 VOCs including methyl butanol, methyl propanol, phenylethanol and thiophene derivatives. The origin of the VOCs is unclear (5–6). Ectosymbiotic bacteria (H) of Fusarium oxysporum(I) and lettuce (L): β-caryophyllene (9) produced by F. oxysporum WT MSA35 (H + I) has a plant growth-promoting effect on lettuce (L); WT F. oxysporum (H + I) produces unknown VOCs (8) that inhibit the growth of phytopathogenic fungi (M). Table 1. Volatile organic compounds involved in the fungal symbioses (the subject of this review) highlighting the producer and the receiver. Plant/fungal/bacterial species . Host . VOC . Origin . Effect on the interaction . Reference . Bean and carrot roots Gigaspora gigantea Unknown Unclear Germination of AM spores and growth of the hyphae towards the plant roots Koske 1982 Gigaspora margarita Lotus japonicus Arabidopsis thaliana Unknown Unclear Increased number and intensity of plant lateral roots Sun, Bonfante and Tang 2015 Gigaspora margarita Lotus japonicus Unknown Unclear Modification of the branch angle of plant lateral roots; enhancement of plant strigolactones production Sun, Bonfante and Tang 2015 Tuber borchii Tilla americana 2-undecenal-2ethyl-1 dodecanol; 2,4-hexadien-1-ol; 2-ethylcrotonaldhehyde; 2-propylheptanol; germacrene D Plant Increasing of fungal growth Menotta et al. 2004 Tuber borchii Tilla americana Dehydroaromadendrene; β-cubebene; longiclyene Plant Chemotropism of fungal hyphae towards plant roots Menotta et al. 2004 Tuber borchii Tilla americana 2,3-dimethyldecane; p-isopropylbenzaldehyde; 1-pentanol Unclear Unknown role in the interaction Menotta et al. 2004 Laccaria bicolor Populus Thujopsene Fungus Lateral root formation Increasing of root hair length superoxide anion radical formation in root tips Ditengou et al. 2015 Tuber aestivum; Tuber borchii; Tuber melanosporum plus their bacterial community / Methylbutanol; methylpropanil; phenylethanol; thujopsene derivatives Unclear Attraction of mammals for the spread of fungal spores Splivallo et al. 2011 Fusarium oxysporum f.sp.lactucae plus its bacterial community Lactuca sativa β-caryophyllene Fungus Plant growth Minerdi et al. 2011 Fusarium oxysporum f.sp.lactucae plus its bacterial community Fusarium oxysporum Unknown Unclear Hydrophobicity of fungal hyphae Minerdi et al. 2009 Fusarium oxysporum f.sp.lactucae plus its bacterial community Pathogenic formae speciales of Fusarium oxysporum Unknown Unclear Repression of fungal virulence genes; reduced mycelial growth Minerdi et al. 2008 Mortierella elongata Mycoavidus cysteinexygens Alcohols; aldehydes; ketones; furans Unclear Increasing VOCs production Uehling et al.2017 Plant/fungal/bacterial species . Host . VOC . Origin . Effect on the interaction . Reference . Bean and carrot roots Gigaspora gigantea Unknown Unclear Germination of AM spores and growth of the hyphae towards the plant roots Koske 1982 Gigaspora margarita Lotus japonicus Arabidopsis thaliana Unknown Unclear Increased number and intensity of plant lateral roots Sun, Bonfante and Tang 2015 Gigaspora margarita Lotus japonicus Unknown Unclear Modification of the branch angle of plant lateral roots; enhancement of plant strigolactones production Sun, Bonfante and Tang 2015 Tuber borchii Tilla americana 2-undecenal-2ethyl-1 dodecanol; 2,4-hexadien-1-ol; 2-ethylcrotonaldhehyde; 2-propylheptanol; germacrene D Plant Increasing of fungal growth Menotta et al. 2004 Tuber borchii Tilla americana Dehydroaromadendrene; β-cubebene; longiclyene Plant Chemotropism of fungal hyphae towards plant roots Menotta et al. 2004 Tuber borchii Tilla americana 2,3-dimethyldecane; p-isopropylbenzaldehyde; 1-pentanol Unclear Unknown role in the interaction Menotta et al. 2004 Laccaria bicolor Populus Thujopsene Fungus Lateral root formation Increasing of root hair length superoxide anion radical formation in root tips Ditengou et al. 2015 Tuber aestivum; Tuber borchii; Tuber melanosporum plus their bacterial community / Methylbutanol; methylpropanil; phenylethanol; thujopsene derivatives Unclear Attraction of mammals for the spread of fungal spores Splivallo et al. 2011 Fusarium oxysporum f.sp.lactucae plus its bacterial community Lactuca sativa β-caryophyllene Fungus Plant growth Minerdi et al. 2011 Fusarium oxysporum f.sp.lactucae plus its bacterial community Fusarium oxysporum Unknown Unclear Hydrophobicity of fungal hyphae Minerdi et al. 2009 Fusarium oxysporum f.sp.lactucae plus its bacterial community Pathogenic formae speciales of Fusarium oxysporum Unknown Unclear Repression of fungal virulence genes; reduced mycelial growth Minerdi et al. 2008 Mortierella elongata Mycoavidus cysteinexygens Alcohols; aldehydes; ketones; furans Unclear Increasing VOCs production Uehling et al.2017 Open in new tab Table 1. Volatile organic compounds involved in the fungal symbioses (the subject of this review) highlighting the producer and the receiver. Plant/fungal/bacterial species . Host . VOC . Origin . Effect on the interaction . Reference . Bean and carrot roots Gigaspora gigantea Unknown Unclear Germination of AM spores and growth of the hyphae towards the plant roots Koske 1982 Gigaspora margarita Lotus japonicus Arabidopsis thaliana Unknown Unclear Increased number and intensity of plant lateral roots Sun, Bonfante and Tang 2015 Gigaspora margarita Lotus japonicus Unknown Unclear Modification of the branch angle of plant lateral roots; enhancement of plant strigolactones production Sun, Bonfante and Tang 2015 Tuber borchii Tilla americana 2-undecenal-2ethyl-1 dodecanol; 2,4-hexadien-1-ol; 2-ethylcrotonaldhehyde; 2-propylheptanol; germacrene D Plant Increasing of fungal growth Menotta et al. 2004 Tuber borchii Tilla americana Dehydroaromadendrene; β-cubebene; longiclyene Plant Chemotropism of fungal hyphae towards plant roots Menotta et al. 2004 Tuber borchii Tilla americana 2,3-dimethyldecane; p-isopropylbenzaldehyde; 1-pentanol Unclear Unknown role in the interaction Menotta et al. 2004 Laccaria bicolor Populus Thujopsene Fungus Lateral root formation Increasing of root hair length superoxide anion radical formation in root tips Ditengou et al. 2015 Tuber aestivum; Tuber borchii; Tuber melanosporum plus their bacterial community / Methylbutanol; methylpropanil; phenylethanol; thujopsene derivatives Unclear Attraction of mammals for the spread of fungal spores Splivallo et al. 2011 Fusarium oxysporum f.sp.lactucae plus its bacterial community Lactuca sativa β-caryophyllene Fungus Plant growth Minerdi et al. 2011 Fusarium oxysporum f.sp.lactucae plus its bacterial community Fusarium oxysporum Unknown Unclear Hydrophobicity of fungal hyphae Minerdi et al. 2009 Fusarium oxysporum f.sp.lactucae plus its bacterial community Pathogenic formae speciales of Fusarium oxysporum Unknown Unclear Repression of fungal virulence genes; reduced mycelial growth Minerdi et al. 2008 Mortierella elongata Mycoavidus cysteinexygens Alcohols; aldehydes; ketones; furans Unclear Increasing VOCs production Uehling et al.2017 Plant/fungal/bacterial species . Host . VOC . Origin . Effect on the interaction . Reference . Bean and carrot roots Gigaspora gigantea Unknown Unclear Germination of AM spores and growth of the hyphae towards the plant roots Koske 1982 Gigaspora margarita Lotus japonicus Arabidopsis thaliana Unknown Unclear Increased number and intensity of plant lateral roots Sun, Bonfante and Tang 2015 Gigaspora margarita Lotus japonicus Unknown Unclear Modification of the branch angle of plant lateral roots; enhancement of plant strigolactones production Sun, Bonfante and Tang 2015 Tuber borchii Tilla americana 2-undecenal-2ethyl-1 dodecanol; 2,4-hexadien-1-ol; 2-ethylcrotonaldhehyde; 2-propylheptanol; germacrene D Plant Increasing of fungal growth Menotta et al. 2004 Tuber borchii Tilla americana Dehydroaromadendrene; β-cubebene; longiclyene Plant Chemotropism of fungal hyphae towards plant roots Menotta et al. 2004 Tuber borchii Tilla americana 2,3-dimethyldecane; p-isopropylbenzaldehyde; 1-pentanol Unclear Unknown role in the interaction Menotta et al. 2004 Laccaria bicolor Populus Thujopsene Fungus Lateral root formation Increasing of root hair length superoxide anion radical formation in root tips Ditengou et al. 2015 Tuber aestivum; Tuber borchii; Tuber melanosporum plus their bacterial community / Methylbutanol; methylpropanil; phenylethanol; thujopsene derivatives Unclear Attraction of mammals for the spread of fungal spores Splivallo et al. 2011 Fusarium oxysporum f.sp.lactucae plus its bacterial community Lactuca sativa β-caryophyllene Fungus Plant growth Minerdi et al. 2011 Fusarium oxysporum f.sp.lactucae plus its bacterial community Fusarium oxysporum Unknown Unclear Hydrophobicity of fungal hyphae Minerdi et al. 2009 Fusarium oxysporum f.sp.lactucae plus its bacterial community Pathogenic formae speciales of Fusarium oxysporum Unknown Unclear Repression of fungal virulence genes; reduced mycelial growth Minerdi et al. 2008 Mortierella elongata Mycoavidus cysteinexygens Alcohols; aldehydes; ketones; furans Unclear Increasing VOCs production Uehling et al.2017 Open in new tab Expression profile analysis of the genes involved in mycorrhization establishment and root development in Lo. japonicus has revealed the upregulation of strigolactone biosynthetic pathway under exposure to bVOCs synthesized by germinating spores. Strigolactones stimulate AM fungal hyphal branching (Besserer et al. 2006) and release short fungal chito-oligosaccharides that are important factors for early plant-fungal communication (Genre et al. 2013). Fungal VOCs enhance the synthesis of plant strigolactones and thus their release in the rhizosphere allows AM fungal hyphae to localize the plant root (Sun, Bonfante and Tang 2015). VOCs in ectomycorrhizae EM symbioses are mutualistic associations occurring between basidiomycetes and ascomycetes and gymnosperms and angiosperms (Taylor and Bruns 1997). The fungus develops around short roots generating a network of intercellular hyphae between the epidermal and cortical cells, increasing the contact area between the fungus and the host plant (Fig. 2D). EM formation requires a very complex signaling dialogue between the fungus and its host. An interesting example of such interactions is represented by the ascomycetous fungus Tuber borchii forming EM with the roots of angiosperms and gymnosperms; this interaction is required for the formation of the fruit body (i.e. the truffle) (Fig. 2G). It has been reported that (at least) 29 volatile molecules including aldehydes, ketones and alcohols are synthesized when Tu. borchii and the host plant Tilia americana interact in the pre-symbiotic stage to form an ectomycorrhiza (Menotta et al. 2004) (Table 1) (Fig. 2D-E-3–4); however, it is not still clear which VOCs are synthesized by the fungus and/or by the plant. It has been shown that the aldehydes 2‐undecenal, 2‐ethyl‐1‐dodecanol, 2,4‐hexadien‐1‐ol, 2‐ethylcrotonaldehyde, 2‐propylheptanol and the sesquiterpene germacrene D (Fig. 1C) (Table 1) might improveTu. borchii growth as already reported for Aspergillus flavus (Zeringue and Mccormick 1989). The terpenoids dehydroaromadendrene, β‐cubebene and longicyclene (Fig. 1C) (Table 1) produced during EM pre‐symbiotic interaction might be related to chemotropism of Tu. borchii hyphae towards the roots of Ti. americana as found in the case of the Pinus sylvestris roots (Fries et al. 1987). The terpenoid molecules 2,3‐dimethyldecane, p‐isopropylbenzaldehyde and 1‐pentanol (Fig. 1C) (Table 1), detected during the interaction of Tu. borchii and Ti. americana, might play some role in this interaction since the dimethyl group is present in several plant semiochemical terpenoids (Menotta et al. 2004). In fact, these molecules are the best diffusing compounds in the soil (Hiltpold and Turlings 2008), strongly suggesting that they might represent good candidates for below-ground signaling. According to this idea, Ditengou and colleagues (2015) have demonstrated that these molecules play a role in the early communication steps between EM fungus Laccaria bicolor and the roots of the host plant Populus (Fig. 2D-E-3–4). Indeed, the sequiterpene thujopsene synthesized by the fungus promotes Populus lateral root formation and also increases the root hair length (Fig. 2D-E-3–4) (Table 1). This effect enhances the area of root surface for the uptake of plant nutrient and improves the access to carbon derived from the plant. The inhibition of fungal sesquiterpene production by lovastatin reduces lateral root formation. Thujopsene also promotes superoxide anion radical formation in the meristematic zone of root tips. VOCs in the symbiosis of fungi with bacteria The role of VOCs in the interaction(s) between fungi and free-living soil bacteria is well documented (Effmert et al. 2012; Schmidt et al. 2016; Schulz-Bohm, Martín-Sánchez and Garbeva 2017). Volatiles emitted by bacteria belong to different classes, such as ketones, esters, lactones, sulphides, alkanes, pyrazines and alkenes (Wenke et al. 2012) and can have different effects on fungi, such as: inhibition of fungal spore germination and mycelial growth of plant pathogens by rhizobacterial VOCs (Zou et al. 2007; Babaeipoor et al. 2011; Logeshwarm et al. 2011); modulation of the mycorrhizal fungi growth and spore germination (Tylka, Hussey and Roncadori 1991; Horii and Ishii 2006); modification of fungal morphology (Barbieri et al. 2005; Zhao et al. 2011), enzyme activity (Crowe and Olsson 2001; Minerdi et al. 2009; Zhao et al. 2011) and gene expression (Kai et al. 2010; Schmidt et al. 2017). Fungal VOCs can play an important role in long distance fungal–bacterial interactions and can lead to different phenotypical responses in the interacting partners. Trichoderma atroviride emits VOCs that increase the expression of the biocontrol gene encoding the biosynthesis of 2,4-diacetylphloroglucinol in Pseudomonas fluorescens (Lutz et al. 2004). The oyster mushroom Pleurotus ostreatus produces volatiles with inhibitory effects on Bacillus cereus and Bacillus subtilis (Pauliuc and Botǎu 2013). Growth alteration, antimicrobial activity, biofilm formation or motility, swimming and swarming of different soil bacterial strains are significantly positively or negatively affected by VOCs produced by several fungi and oomycetes (Schmidt et al. 2015). Serratia plymuthica exposed to VOCs emitted by the fungal pathogen Fusarium culmorum showed that the bacterium responds to the fungal volatiles, changing the gene and protein expression related to motility, signal transduction, energy metabolism, cell envelope biogenesis and secondary metabolite production (Schmidt et al. 2017). The new eukaryotic/prokaryotic entity has its own VOCs profile When an ecto/endosymbiotic association takes place, a new biological entity is formed by the fusion of the prokaryotic and fungal partners. The new entity synthesizes a VOCs mixture, which is not the sum of the molecules produced by each partner. It is possible that newly synthesized molecules are useful for the maintenance of the symbiosis and also influence the behavior of other soil organisms including bacteria, fungi and plants. Recent work indicates that the emission of particular volatiles can be induced by the presence of interacting partners not necessarily symbionts, as in the case of the rhizospheric bacterium Se. plymuthica, which modify its mobility and produce the volatile sodorefin in response to the exposure of the volatiles produced by the soil fungus F. culmorum (Schmidt et al. 2017). This suggests a complex regulation of the synthesis and/or emission of volatile molecules rather than an unspecific release of metabolic waste ‘products’. Some examples of the VOCs profiles produced by newly formed symbiotic bacteria-fungi entities and their ecological effects are given below. Truffles and their symbiotic bacteria EM truffles and fruiting bodies host different bacteria (Antony-Babu et al. 2013). It has been shown that Tuber aestivum (Gryndler et al. 2013), Tuber melonosporum (Antony-Babu et al. 2013) and Tu. borchii (Barbieri et al. 2007) share their lives with complex bacterial communities (Fig. 2F). The peridium and the gleba of fruiting bodies (Fig. 2G) harbor soil bacterial communities (Fig. 2F) during the early stages of truffle formation (Antony-Babu et al. 2013). The role played by these bacterial communities in symbiosis is not fully understood; for instance, they might contribute to nitrogen fixation, cellulose and chitin degradation and/or sulphur metabolism. Fruiting bodies emit a complex mixture of almost 50 VOCs (Splivallo et al. 2011), including methyl butanol, methyl propanol, phenylethanol and thiophene derivatives (Table 1) (Fig. 1D) (Fig. 2F-G-5–6). The typical aroma of truffles is due to thiophene volatiles that attract mammals in order to spread the fungal spores (Cullerè et al. 2010). This class of VOCs derives from non-volatile precursors produced by the interaction between bacteria, yeasts and truffles (Splivallo and Eberl 2015). Fusarium oxysporum f. sp. lactucae and its microbial community The antagonistic wild-type (WT) Fusarium oxysporum (Fig. 2H+I) strain MSA35 hosts ectosymbiotic bacteria (Fig. 2H) belonging to the genera Serratia, Achromobacter, Bacillus and Stenotrophomonas on the surface of its hyphae. When the WT form is cured of the bacterial symbionts (CU form), it becomes pathogenic towards lettuce (Minerdi et al. 2008). It has been shown that sesquiterpens like icaryophyllene, α-humulene and cyclocaryophyllan-4-ol (Table 1) (Figs 1F and 2H-I) are produced only by the WT form; hence, it is still not clear whether the VOCs are synthesized by Fusarium, ectosymbiotic bacteria or by the new entity formed by their interaction. Moreover, it has been shown that butylate hydroxyanisole (Fig. 1E) and isolongifolene (Fig. 1F) (Table 1) are synthesized in higher quantities in the F. oxysporum CU strain than in the WT one; on the contrary, longipinalol is produced only by the CU strain (Minerdi et al. 2008). Hence, the fungus with its bacteria (2h+i) produces unknown VOCs (-8), limiting mycelial growth and repressing the expression of virulence genes of different pathogenic formae speciales of F. oxysporum (Fig. 2M). None of the VOCs produced by the cultivable ectosymbiotic bacteria have an effect on the growth of lettuce seedlings. On the contrary, β-caryophyllene (Figs 1F and 2–9) (Table 1) produced by F. oxysporum WT MSA35 (Fig. 2H+I) has a plant-growth promoting effect on lettuce (Minerdi et al. 2011). VOCs from WT MSA35 are also able to influence the phenotype of MSA35 mycelium: hyphae grown in their presence are hydrophobic whereas those grown without VOCs are hydrophilic with an altered ability to attach to the root surface and enter the plant (Minerdi et al. 2009). Fungal endobacteria Bacteria living inside fungal cells (endofungal bacteria) are omnipresent in fungi belonging to different taxa and with diverse lifestyles ranging from endophytic Ascomycetes (Arendt et al. 2016; Shaffer et al. 2016), saprotrophic and symbiotic Mucoromycota (Uehling et al. 2017; Desirò et al. 2018) to symbiotic, pathogenic and endophytic Basidiomycetes (Glaeser et al2016). The mechanism(s) used by bacteria to colonize their host are known only in a few examples: in those cases chitinolytic enzymes or lipopeptides are produced to enter the fungal host (Moebius et al. 2014). No volatile compound is known to be directly involved in the formation of the endosymbiosis, but also in this situation the new eukaryotic/prokaryotic entity has its own VOCs profile, suggesting a reprogramming of bacterial/fungus metabolic pathways responsible for VOCs biosynthesis. Usually, the endosymbiotic bacteria affect the host metabolism (with still unknown mechanisms), influencing growth (Uehling et al. 2017; Desirò et al. 2018), primary (Vannini et al. 2016; Li et al. 2017) and secondary metabolism (Rohm et al. 2010; Hoffman et al. 2013). The soil fungus Mortierella elongata hosts the endosymbiotic bacterium Mycoavidus cysteinexigens in the hyphal cytoplasm (Ohshima et al. 2016). The fungus cured from the endobacteria and the WT formed produce a different blend of volatiles, both from the point of view of quality and the quantity of the molecules emitted (Uehling et al. 2017). Indeed, the bacteria-free Mo. elongata emits butyric and crotonic acids and their esters, while the fungus hosting My. cysteinexigens synthesizes a high quantity of alcohols, aldehydes, ketones and furans. It is not still clear whether the endobacteria synthesize VOCs by themselves or if their presence/absence influences the fungal metabolism, as shown for plant-bacteria interactions (Maggini et al. 2017a, 2019). In any case, VOCs can influence microbial interactions and chemical ecology in soil and plant rhizosphere (Schulz et al. 2018). POTENTIAL OF fVOCS FOR BIOTECHNOLOGICAL APPLICATIONS Food and/or cosmetic industry In this field, some of the VOCs identified so far are already used as flavoring agents and adjuvant as well as indicators of mold growth in crops and environment, insect attractors or repellents and spore inhibitors (Hung et al. 2015). Methyl butanol is a flavoring agent present in wine; 2,4-hexadien-1-ol, p-isopropylbenzaldehyde, 1-pentanol and 2-undecanone are used in rose, lavender, clary sage and opopanax. Pharmacology It has been already shown that β-caryophyllene, a nonsteroidal anti-inflammatory agent, possesses analgesic, antipyretic and platelet-inhibitory actions, avoiding the synthesis of prostaglandins by inhibiting the cyclooxygenase converting arachidonic acid to cyclic endoperoxides (prostaglandin precursors). Moreover, Legault and Pichette (2007) demonstrated that β-caryophyllene increases the efficacy of commonly used chemotherapy drugs. Agriculture During the last decade, fVOCs have attracted attention in this field due to their promising effect on plant growth improvement and crop protection. Crop protection from pathogens depends on the use of harmful chemical pesticides needing to be replaced/complemented with novel methods of sustainable agriculture (Kanchiswamy, Malnoy and Maffei 2015). For example, fungi are able to transform plant terpenoids implementing plant defenses toward pathogens (Mucciarelli et al. 2007). Currently, bVOCs are used as foliar sprays and by soil dumping in field biocontrol strategies but very few studies have investigated the direct application of the producing strains to the soil in open field to establish a fungal symbiosis producing VOCs in a stable and prolonged manner (Schulz-Bohm, Martín-Sánchez and Garbeva 2017). Unfortunately, the inoculation of biocontrol microbes into soil collides with the competitive exclusion of invader strains by indigenous microbial communities (de Boer 2019). To overcome this kind of microbial competition, the soil could be provided with preferential substrates for biocontrol strains and not easily degraded by the residential microbes. Bio-fuel production Recently, it has been shown that some volatile-producing endophytes, cryptic fungal symbionts persisting in healthy plant tissues, have a rare ability to synthesize carbon chains that are identical to many of those found in petroleum and/or diesel fuel, suggesting that they might contribute to bio-fuel production. Drug discovery The findings reported in the previous four subsections clearly show that, from an application-oriented and biotechnological viewpoint, fVOCs have potential for sustainable development of agriculture, forestry and industry, especially in the control of fruit post-harvest diseases, soil-borne pathogen management and bio-fuel production. However, in our opinion, one of the most interesting applications of fVOCs is their possible use as antimicrobial compounds. This represents a very important issue due to the insurgence of antibiotic resistance and the emergence of multidrug-resistant pathogens prioritizing research to discover new antimicrobials, especially natural compounds from unusual sources (bioprospecting) as marine metazoans (Blunt et al. 2004), or microorganisms from extreme environments like Antarctica (Papaleo et al. 2012, 2013). However, a very interesting and promising source of new natural antibiotics is represented by medicinal plants (e.g. Altintas et al. 2013; Freires et al. 2015; Martins et al. 2015). Indeed, it has been shown that essential oils from different medicinal plants, such as Lavandula officinalis, Origanum vulgare and Thymus (Maida et al. 2014; Pesavento et al. 2016; Checcucci et al. 2017; Maggini et al. 2017b), possess strong antimicrobial activity against different human pathogens resistant to a plethora of antibiotics. The plant VOCs could also boost the antibiotic efficacy as a result of an intracellular mechanism of action, as demonstrated using Burkholderia cepacia mutants affected in efflux pumps (Perrin et al. 2018). It has been recently shown that the aforementioned medicinal plants, as well as Echinacea purpurea and Echinacea angustifolia, harbor complex bacterial communities (Chiellini et al. 2017; Maggini et al. 2020), whose members synthesize VOCs, exhibiting an ability to completely inhibit the growth of many human pathogens, most of which are particularly resistant to the commonly used antibiotics, including the last generation ones (Chiellini et al. 2017; Presta et al. 2017; Garbeva and Weisskopf 2019; Castronovo et al. 2020). Potential application of VOCs to in vitro propagation of AM and ectomycorrhizal fungi The biotrophic and hypogeous nature of the mycobionts complicates the study of AM fungi and their symbiosis with the host plant roots. To overcome this, the in vitro use of root-organ cultures has proved particularly successful (Fortin et al. 2002). The hyphal branching and growth of AM fungus in the pre-symbiotic stage is important since it must find a compatible host to complete its lifecycle. Different environmental factors including light, gaseous or volatile compounds and non-volatile chemicals can affect, singularly or synergistically, the AM fungal growth during this early developmental stage. At present, no data are available about the treatment of root organ cultures with specific VOCs. However, it can be reasonably assumed that the production of AM fungi could greatly be improved by adding the growth medium to the volatile compounds (to be identified) emitted during a symbiotic interaction, such as between Gigaspora margarita and Lo. japonicas (Sun, Bonfante and Tang 2015). Their application should also increase the number and density of host plant lateral roots and direct their branch angle towards germinating spores, increasing the chances of AM hyphae encountering plant roots. A significant proportion of ectomycorrhizal fungal species (many of which are commercially important) form edible fruiting bodies. The most highly regarded ectomycorrhizal fungi include truffles, which have great economic value. The cultivation of an ectomycorrhizal fungus requires the growth of the mycelium on a specific culture substrate in the presence of a suitable plant host to establish the symbiosis and then promote the production of the edible mushrooms. Most of the in vitro mycorrhization techniques applied to edible mushrooms have been developed to obtain mycorrhized plantlets and are then planted to obtain fruiting bodies. To establish the ectomycorrhizal symbiosis, the two partners must exchange some signals to allow mutual recognition (Tagu, Lapeyrie and Martin 2002). In in vitro cultures, it could be useful to add to the growth medium the VOCs dehydroaromadendrene, β‐cubebene and longicyclene, to promote the symbiosis between two partners interacting with no contact. These molecules should direct the growth of Tu. borchii hyphae towards the roots of the host plant Ti. americana. The use of the sequiterpene thujopsene, synthesized by the ectomycorrhizal fungus (Ditengou et al. 2015), should elicit host plant lateral root formation and increase the root hair length by promoting the hyphae-roots interactions. CONCLUSIONS AND OUTLOOK An incessant, increasing number of studies are witnessing the importance of VOCs in long-distance below-ground communication leading to the formation of symbioses between fungi and plants or bacteria. As new interactions between microorganisms and plants and fungi are deciphered, VOCs with new functions will be discovered. To date, any information about the role of VOCs in endosymbiotic fungal-bacterial interactions is reported; it is known that once the symbiosis is established, VOCs are produced to promote biological function(s) that still need(s) to be fully deciphered. A big challenge is represented by the elucidation of the molecular mechanism(s) responsible for: (i) the production of volatiles by a member of the symbiosis, (ii) their perception by the other member(s) of the symbiosis and (iii) the genetic reprogramming of the symbiotic partners, allowing the synthesis of a new VOCs profile different from those exhibited by the single partners alone. Many fundamental questions underlying both the fungal and the plant and bacteria sides of the volatile-mediated interaction remain unexplored. For example, an important knowledge gap is represented by the unrevealed role of VOCs in the formation of well-known symbioses between yeasts and insects (Stefanini 2018) or other putative hosts (Ling et al. 2020). Moreover, very little information is available about the genetic basis of fungal volatile emission, synthesis membrane crossing via specific transporters or through diffusion. Most of our knowledge on the emission of volatiles by fungi and bacteria originates from laboratory studies on single strains. We need to consider that inoculated strains have to integrate into a complex rhizosphere community and that interspecific interactions can strongly influence volatile emission (Tyc, Wolf and Garbeva 2015). For example, volatile emission in bacteria can be induced by the exposition to fungal volatiles (Schmidt et al. 2017). Moving to an unexplored additional level of interaction, Kai and colleagues (2018) demonstrated that bacterial volatile precursors released by a Gram positive chemically reacted in the shared headspace of a Gram negative, yielding a new volatile. This discovery added chemical features to the biological complexity of the microbial interactions. Presumably, the changes in the volatile blend triggered by the addition of volatile-emitting strains to the diverse rhizosphere communities will be very difficult to predict. Another interesting issue is the possibility that fungal VOCs synthesized during the symbiosis may represent some of the molecules composing the plant extracts or essential oils. Moreover, it is also possible that such VOCs may influence the plant metabolism, increasing the production of bioactive compounds. Hence, the isolation and the phenotypic, molecular and genomic characterization of fungi associated with medicinal plants might be of great interest to understand the role they can play in the biosynthesis of volatile compounds existing in medicinal plants extracts/essential oils. In order to try to give an answer to these important questions, it appears pivotal to set up innovative in vitro models able to mimic the natural conditions of fungal symbiosis to compare them with the cultured microorganism grown alone. Actually, a tripartite fungal–algal–bacterial model system has been set up to test the interaction between lichenised fungi and algae and selected bacteria (Muggia et al. 2016). When innovative fungal symbioses in vitro models are set up, this will help to face another big challenge: to understand the possibility to use VOCs from a biotechnological point of view to influence the formation and maintenance of fungal symbioses useful to sustainable agriculture (AM) or to forestry (EM). In conclusion, the role of VOCs to establish fungal symbiosis is undisputed. However, we need extensive research efforts to advance our basic understanding of the mechanisms at the basis of volatile production by the symbiosis partners and to move away from the artificial laboratory to experimental conditions that come closer to the natural fungal symbiosis environment. Conflicts of interest None declared. REFERENCES Agrios GN . Plant pathology . 5th ed. Amsterdam, The Netherlands : Elsevier Academic Press , 2005 , 952 . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Altintas A , Tabanca N, Tyihák E et al. Characterization of volatile constituents from Origanum onites and their antifungal and antibacterial activity . J AOAC Int . 2013 ; 96 : 1200 – 8 . Google Scholar OpenURL Placeholder Text WorldCat Ameztoy K , Baslam M, Sánchez-López ÁM et al. Plant responses to fungal volatiles involve global posttranslational thiol redox proteome changes that affect photosynthesis . Plant Cell Environ . 2019 ; 42 : 2627 – 44 . Google Scholar OpenURL Placeholder Text WorldCat Antony-Babu S , Deveau A, Van Nostrand JD et al. Black truffle associated bacterial communities during the development and maturation of Tuber melanosporum ascocarps and putative functional roles . Environ Microbiol . 2014 ; 16 : 2831 – 47 . Google Scholar OpenURL Placeholder Text WorldCat Arendt KR , Hockett KL, Araldi-Brondolo SJ et al. Isolation of endohyphal bacteria from foliar Ascomycota and in vitro establishment of their symbiotic associations . Appl Environ Microbiol . 2016 ; 82 : 2943 – 9 . Google Scholar OpenURL Placeholder Text WorldCat Auge RM . Water relations, drought and vesicular arbuscular mycorrhizal symbiosis . Mycorrhiza . 2001 ; 11 : 3 – 42 . Google Scholar OpenURL Placeholder Text WorldCat Azcon-Aguilar C , Miguel-Barea J. Nutrient cycling in the mycorrhizosphere . J Soil Sci Plant Nutr . 2015 ; 15 : 372 – 96 . Google Scholar OpenURL Placeholder Text WorldCat Babaeipoor E , Mirzaei S, Danesh YR et al. Evaluation of some antagonistic bacteria in biological control of Gaeumannomyces graminis var tritici causal agent of wheat take-all disease in Iran . Afr J Microbiol Res . 2011 ; 5 : 5165 – 73 . Google Scholar OpenURL Placeholder Text WorldCat Bago B , Pfeffer PE, Shachar-Hill Y. Carbon metabolism and transport in arbuscular mycorrhizas . Plant Physiol . 2000 ; 124 : 949 – 58 . Google Scholar OpenURL Placeholder Text WorldCat Barbieri E , Bertini L, Rossi I et al. New evidence for bacterial diversity in the ascoma of the ectomycorrhizal fungus Tuber borchii Vittad . FEMS Microbiol Lett . 2005 ; 247 : 23 – 35 . Google Scholar OpenURL Placeholder Text WorldCat Barbieri E , Guidi C, Bertaux J et al. Occurrence and diversity of bacterial communities in Tuber magnatum during truffle maturation . Environ Microbiol . 2007 ; 9 : 2234 – 46 . Google Scholar OpenURL Placeholder Text WorldCat Besserer A , Puech-Pages V, Kiefer P et al. Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria . PLoS Biol . 2006 ; 4 : 1239 – 47 . Google Scholar OpenURL Placeholder Text WorldCat Bjurman J . Release of BVOCs from microorganisms . In: Salhammer T (ed.) Organic Indoor Air Pollutants: Occurrence, Measurement, Evaluation . Weinheim, Germany : Wiley-VCH , 1999 , 259 – 73 . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Blom D , Fabbri C, Connor EC et al. Production of plant growth modulating volatiles is widespread among rhizosphere bacteria and strongly depends on culture conditions . Environ Microbiol . 2011 ; 13 : 3047 – 58 . Google Scholar OpenURL Placeholder Text WorldCat Blunt JW , Copp BR, Munro MH et al. Marine natural products . Nat Prod Rep . 2004 ; 21 : 1 – 49 . Google Scholar OpenURL Placeholder Text WorldCat Castronovo LM , Calonico C, Ascrizzi R et al. The cultivable bacterial microbiota associated to the medicinal plant Origanum vulgare L.: from antibiotic resistance to growth-inhibitory properties . Front Microbiol . 2020 ; 11 : 1 – 17 . Google Scholar OpenURL Placeholder Text WorldCat Checcucci A , Maida I, Bacci G et al. Is the plant-associated microbiota of Thymus spp. adapted to the plant essential oil? Res Microbiol . 2017 ; 168 : 276 – 82 . Google Scholar OpenURL Placeholder Text WorldCat Chen H , Fink GR. Feedback control of morphogenesis in fungi by aromatic alcohols . Genes Dev . 2006 ; 20 : 1150 – 61 . Google Scholar OpenURL Placeholder Text WorldCat Chiellini C , Maida I, Maggini V et al. Preliminary data on antibacterial activity of Echinacea purpurea-associated bacterial communities against Burkholderia cepacia complex strains, opportunistic pathogens of cystic fibrosis patients . Microbiol Res . 2017 ; 196 : 34 – 43 . Google Scholar OpenURL Placeholder Text WorldCat Chiron N , Michelot D. Odeurs de champignons: chimie et role dans les interactions biotiques- une revue . Cryptogam Mycol . 2005 ; 26 : 299 – 364 . Google Scholar OpenURL Placeholder Text WorldCat Chuankun X , Minghe M, Leming Z et al. Soil volatile fungistasis and volatile fungistatic compounds . Soil Biol Biochem . 2004 ; 36 : 1997 – 2004 . Google Scholar OpenURL Placeholder Text WorldCat Cordovez V , Mommer L, Moisan K et al. Plant phenotypic and transcriptional changes induced by volatiles from the fungal root pathogen rhizoctonia solani . Front Plant Sci . 2017 ; 8 : 1262 . Google Scholar OpenURL Placeholder Text WorldCat Crowe JD , Olsson S. Induction of laccase activity in Rhizoctonia solani by antagonistic Pseudomonas fluorescens strains and a range of chemical treatments . Appl Environ Microbiol . 2001 ; 67 : 2088 – 94 . Google Scholar OpenURL Placeholder Text WorldCat Cullere L , Ferreira V, Chevret B et al. Characterisation of aroma active compounds in black truffles (Tuber melanosporum) and summer truffles (Tuber aestivum) by gas chromatography-olfactometry . Food Chem . 2010 ; 122 : 300 – 6 . Google Scholar OpenURL Placeholder Text WorldCat de Boer W , Li X, Meisner A et al. Pathogen suppression by microbial volatile organic compounds in soils . FEMS Microbiol Ecol . 2019 ; 95 : fiz105 . Google Scholar OpenURL Placeholder Text WorldCat Desirò A , Hao Z, Liber JA et al. Mycoplasma-related endobacteria within Mortierellomycotina fungi: diversity, distribution and functional insights into their lifestyle . ISME J . 2018 ; 12 : 1743 – 57 . Google Scholar OpenURL Placeholder Text WorldCat Ditengou FA , Muller A, Rosenkranz M et al. Volatile signalling by sesquiterpenes from ectomycorrhizal fungi reprogrammes root architecture . Nat Commun . 2015 ; 6 : 6279 . Google Scholar OpenURL Placeholder Text WorldCat Dixon EF , Hall RA. Noisy neighbourhoods: quorum sensing in fungal-polymicrobial infections . Cell Microbiol . 2015 ; 17 : 1431 – 41 . Google Scholar OpenURL Placeholder Text WorldCat Dunkel M , Schmidt U, Struck S et al. SuperScent-a database of flavors and scents . Nucleic Acids Res . 2009 ; 37 : D291 – 4 . Google Scholar OpenURL Placeholder Text WorldCat Effmert U , Buss D, Rohrbeck D et al. Localization of the synthesis and emission of scent compounds within the flower . Biol Floral Scent . 2006 ; 105 – 24 . Google Scholar OpenURL Placeholder Text WorldCat Effmert U , Kalderas J, Warnke R et al. Volatile mediated interactions between bacteria and fungi in the soil . J Chem Ecol . 2012 ; 38 : 665 – 703 . Google Scholar OpenURL Placeholder Text WorldCat Feeney DS , Crawford JW, Daniell T et al. Three-dimensional microorganization of the soil-root-microbe system . Microb Ecol . 2006 ; 52 : 151 – 8 . Google Scholar OpenURL Placeholder Text WorldCat Fiedler K , Schuetz E, Geh S. Detection of microbial volatile organic compounds (BVOCs) produced by moulds on various materials . Int J Hyg Environ Health . 2001 ; 204 : 111 – 21 . Google Scholar OpenURL Placeholder Text WorldCat Fischer G , Schwalbe R, Möller M et al. Species-specific production on microbial volatile organic compounds (BVOC) by airborne fungi from a compost facility . Chemosphere . 1999 ; 39 : 795 – 810 . Google Scholar OpenURL Placeholder Text WorldCat Fortin JA , Bécard G, Declerck S et al. Arbuscular mycorrhiza on root-organ cultures . Can J Bot . 2002 ; 80 : 1 – 20 . Google Scholar OpenURL Placeholder Text WorldCat Freires IA , Denny C, Benso B et al. Antibacterial activity of essential oils and their isolated constituents against cariogenic bacteria: a systematic review . Molecules . 2015 ; 20 : 7329 – 58 . Google Scholar OpenURL Placeholder Text WorldCat Fries N , Serckhanssen K, Dimberg IH et al. Abietic acid, an activator of basidiospore germination in ectomycorrhizal species of the genus Suillus (boletaceae) . Exp Mycol . 1987 ; 11 : 360 – 3 . Google Scholar OpenURL Placeholder Text WorldCat Fusconi A . Regulation of root morphogenesis in arbuscular mycorrhizae: what role do fungal exudates, phosphate, sugars and hormones play in lateral root formation? Ann Bot . 2014 ; 113 : 19 – 33 . Google Scholar OpenURL Placeholder Text WorldCat Garbeva P , Weisskopf L. Airborne medicine: bacterial volatiles and their influence on plant health . New Phytol . 2020 ; 226 : 32 – 43 . Google Scholar OpenURL Placeholder Text WorldCat Genre A , Chabaud M, Balzergue C et al. Short-chain chitin oligomers from arbuscular mycorrhizal fungi trigger nuclear Ca2 spiking in Medicago truncatula roots and their production is enhanced by strigolactone . New Phytol . 2013 ; 198 : 190 – 202 . Google Scholar OpenURL Placeholder Text WorldCat Glaeser SP , Imani J, Alabid I et al. Non-pathogenic Rhizobium radiobacter F4 deploys plant beneficial activity independent of its host Piriformospora indica . ISME J . 2016 ; 10 : 871 – 84 . Google Scholar OpenURL Placeholder Text WorldCat Gomes AA , Pinho DB, Cardeal ZL et al. Simplicillium coffeanum, a new endophytic species from Brazilian coffee plants, emitting antimicrobial volatiles . Phytotaxa . 2018 ; 333 : 188 – 98 . Google Scholar OpenURL Placeholder Text WorldCat Groenhagen U , Baumgartner R, Bailly A et al. Production of bioactive volatiles by different Burkholderia ambifaria strains . J Chem Ecol . 2013 ; 39 : 892 – 906 . Google Scholar OpenURL Placeholder Text WorldCat Gryndler ML , Soukupová H, Hršelová H et al. A quest for indigenous truffle helper prokaryotes . Environ Microbiol Rep . 2013 ; 5 : 346 – 52 . Google Scholar OpenURL Placeholder Text WorldCat Gutjahr C , Parniske M. Cell and developmental biology of the arbuscular mycorrhiza symbiosis . Annu Rev Cell Dev Biol . 2013 ; 29 : 593 – 617 . Google Scholar OpenURL Placeholder Text WorldCat Hammerbacher A , Kandasamy D, Ullah C et al. Flavanone-3-hydroxylase plays an important role in the biosynthesis of spruce phenolic defenses against bark beetles and their fungal associates . Front Plant Sci . 2019 ; 10 : 208 . Google Scholar OpenURL Placeholder Text WorldCat Hiltpold I , Turlings TCJ. Belowground chemical signaling in maize: when simplicity rhymes with efficiency . J Chem Ecol . 2008 ; 34 : 628 – 35 . Google Scholar OpenURL Placeholder Text WorldCat Hoffman MT , Gunatilaka MK, Wijeratne K et al. Endohyphal bacterium enhances production of indole-3-acetic acid by a foliar fungal endophyte . PLoS One . 2013 ; 8 : e73132 . Google Scholar OpenURL Placeholder Text WorldCat Hogan DA . Talking to themselves: autoregulation and quorum sensing in fungi . Eukaryotic Cell . 2006 ; 5 : 613 – 9 . Google Scholar OpenURL Placeholder Text WorldCat Horii S , Ishii T. Identification and function of Gigaspora margarita growth-promoting microorganisms . Symbiosis . 2006 ; 41 : 135 – 41 . Google Scholar OpenURL Placeholder Text WorldCat Hornby JM , Jensen ECA, Lisec D et al. Quorum sensing in the dimorphic fungus Candida albicans is mediated by farnesol . Appl Environ Microbiol . 2001 ; 67 : 2982 – 92 . Google Scholar OpenURL Placeholder Text WorldCat Hung R , Lee S, Bennett JW. Fungal volatile organic compounds and their role in ecosystems . Appl Microbiol Biotechnol . 2015 ; 99 : 3395 – 405 . Google Scholar OpenURL Placeholder Text WorldCat Hynes J , Carsten T, Müller T et al. Changes in volatile production during the course of fungal mycelial interactions between Hypholoma fasciculare and Resinicium bicolor . J Chem Ecol . 2006 ; 33 : 43 – 57 . Google Scholar OpenURL Placeholder Text WorldCat Kai M , Crespo E, Cristescu SM et al. Serratia odorifera: analysis of volatile emission and biological impact of volatile compounds on Arabidopsis thaliana . Appl Microbiol Biotechnol . 2010 ; 88 : 965 – 76 . Google Scholar OpenURL Placeholder Text WorldCat Kai M , Effmert U, Lemfack MC et al. Interspecific formation of the antimicrobial volatile schleiferon . Sci Rep . 2018 ; 8 : e16852 . Google Scholar OpenURL Placeholder Text WorldCat Kanchiswamy CN , Malnoy M, Maffei ME. Bioprospecting bacterial and fungal volatiles for sustainable agriculture . Trends Plant Sci . 2015 ; 20 : 206 – 11 . Google Scholar OpenURL Placeholder Text WorldCat Korpi A , Jarnberg J, Pasanen AL. Microbial volatile organic compounds . Crit Rev Toxicol . 2009 ; 39 : 139 – 93 . Google Scholar OpenURL Placeholder Text WorldCat Koske RE . Evidence for a volatile attractant from plant roots affecting germ tubes of a VA mycorrhizal fungus . Trans Br Mycol Soc . 1982 ; 79 : 305 – 10 . Google Scholar OpenURL Placeholder Text WorldCat Kottb M , Gigolashvili T, Großkinsky DK et al. Trichoderma volatiles effecting Arabidopsis: from inhibition to protection against phytopathogenic fungi . Front Microbiol . 2015 ; 6 : 1 – 14 . Google Scholar OpenURL Placeholder Text WorldCat Lee S , Yap M, Behringer G et al. Volatile organic compounds emitted by Trichoderma species mediate plant growth . Fungal Biol Biotechnol . 2016 ; 3 : 7 . Google Scholar OpenURL Placeholder Text WorldCat Legault J , Pichette A. Potentiating effect of beta-caryophyllene on anticancer activity of alpha-humulene, isocaryophyllene and paclitaxel . J Pharm Pharmacol . 2010 ; 59 : 1643 – 7 . Google Scholar OpenURL Placeholder Text WorldCat Lemfack MC , Gohlke BO, Toguem SMT et al. bVOC 2.0: a database of microbial volatiles . Nucleic Acids Res . 2018 ; 46 : D1261 – 5 . Google Scholar OpenURL Placeholder Text WorldCat Létoffé S , Audrain B, Bernier SP et al. Aerial exposure to the bacterial volatile compound trimethylamine modifies antibiotic resistance of physically separated bacteria by raising culture medium pH . MBio . 2014 ; 7 : e00944 – 13 . Google Scholar OpenURL Placeholder Text WorldCat Ling L , Tu Y, Ma W et al. A potentially important resource: endophytic yeasts . World J Microbiol Biotechnol . 2020 ; 36 : 110 . Google Scholar OpenURL Placeholder Text WorldCat Li Z , Yao Q, Dearth SP et al. Integrated proteomics and metabolomics suggests symbiotic metabolism and multimodal regulation in a fungal-endobacterial system . Environ Microbiol . 2017 ; 19 : 1041 – 53 . Google Scholar OpenURL Placeholder Text WorldCat Logeshwarn P , Thangaraju M, Rajasundari K. Antagonistic potential of Gluconacetobacter diazotrophicus against Fusarium oxysporum in sweet potato (Ipomea batatus) . Arch Phytopathol Plflanzenschutz . 2011 ; 44 : 216 – 23 . Google Scholar OpenURL Placeholder Text WorldCat Lutz MP , Wenger S, Maurhofer M et al. Signaling between bacterial and fungal biocontrol agents in a strain mixture . FEMS Microbiol Ecol . 2004 ; 48 : 447 – 55 . Google Scholar OpenURL Placeholder Text WorldCat Maffei ME , Gertsch J, Appendino G. Plant volatiles: production, function and pharmacology . Nat Prod Rep . 2011 ; 28 : 1359 – 80 . Google Scholar OpenURL Placeholder Text WorldCat Maggini V , De Leo M, Granchi C et al. The influence of Echinacea purpurea leaf microbiota on chicoric acid level . Sci Rep . 2019 ; 9 : 10897 . Google Scholar OpenURL Placeholder Text WorldCat Maggini V , De Leo M, Mengoni A et al. Plant-endophytes interaction influences the secondary metabolism in Echinacea purpurea (L.) Moench: an in vitro model . Sci Rep . 2017a ; 7 : 16924 . Google Scholar OpenURL Placeholder Text WorldCat Maggini V , Mengoni A, Bogani P et al. Promoting model systems of microbiota-medicinal plant interactions . Trends Plant Sci . 2020 ; 25 : 223 – 5 . Google Scholar OpenURL Placeholder Text WorldCat Maggini V , Pesavento G, Maida I et al. Exploring the effect of the composition of three different Oregano essential oils on the growth of multidrug-resistant cystic fibrosis Pseudomonas aeruginosa strains . Nat Prod Commun . 2017b ; 12 : 1949 – 52 . Google Scholar OpenURL Placeholder Text WorldCat Maida I , Lo Nostro A, Pesavento G et al. Exploring the anti-Burkholderia cepacia complex activity of essential oils: a preliminary analysis . Evid Based Complement Alternat Med . 2014 ; 201 : 573518 . Google Scholar OpenURL Placeholder Text WorldCat Martins Cde M , do Nascimento EA, de Morais SA et al. Chemical constituents and evaluation of antimicrobial and cytotoxic activities of Kielmeyera coriacea Mart. & Zucc. Essential Oils . Evid Based Complement Altern Med . 2015 ; 2015 : 842047 . Google Scholar OpenURL Placeholder Text WorldCat Mason S , Cortes D, Horner WE. Detection of gaseous effluents and by-products of fungal growth that affect environments . HVAC&R . 2010 ; 10 : 109 – 21 . Google Scholar OpenURL Placeholder Text WorldCat Mburu DM , Ndung'u MW, Maniania NK et al. Comparison of volatile blends and gene sequences of two isolates of Metarhizium anisopliae of different virulence and repellency toward the termite Macrotermes michaelseni . J Exp Biol . 2011 ; 214 : 956 – 62 . Google Scholar OpenURL Placeholder Text WorldCat Menotta M , Gioacchini A, Amicucci A et al. Headspace solid-phase microextraction with gas chromatography and mass spectrometry in the investigation of volatile organic compounds in an ectomycorrhizae synthesis system . Rapid Commun Mass Spectrom . 2004 ; 18 : 206 – 10 . Google Scholar OpenURL Placeholder Text WorldCat Minerdi D , Bossi S, Gullino ML et al. A Volatile organic compounds: a potential direct long-distance mechanism for antagonistic action of Fusarium oxysporum strain MSA35 . Environ Microbiol . 2009 ; 11 : 844 – 54 . Google Scholar OpenURL Placeholder Text WorldCat Minerdi D , Bossi S, Maffei ME et al. Fusarium oxysporum and its bacterial consortium promote lettuce growth and expansin A5 gene expression through microbial volatile organic compound (BVOC) emission . FEMS Microbiol Ecol . 2011 ; 76 : 342 – 51 . Google Scholar OpenURL Placeholder Text WorldCat Minerdi D , Moretti M, Gilardi G et al. Bacterial ectosymbionts and virulence silencing in a Fusarium oxysporum strain . Environ Microbiol . 2008 ; 10 : 1725 – 41 . Google Scholar OpenURL Placeholder Text WorldCat Moebius N , Uzüm Z, Dijksterhuis J et al. Active invasion of bacteria into living fungal cells . eLife . 2014 ; 3 : e03007 . Google Scholar OpenURL Placeholder Text WorldCat Montoya JM , Pimm SL, Sole RV. Ecological networks and their fragility . Nature . 2006 ; 442 : 259 – 64 . Google Scholar OpenURL Placeholder Text WorldCat Mucciarelli M , Camusso W, Maffei M et al. Volatile terpenoids of endophyte-free and infected peppermint (Mentha piperita L.): chemical partitioning of a symbiosis . Microb Ecol . 2007 ; 54 : 685 – 96 . Google Scholar OpenURL Placeholder Text WorldCat Muggia L , Fleischhacker A, Kopun T et al. Extremotolerant fungi from alpine rock lichens and their phylogenetic relationships . Fungal Diversity . 2016 ; 76 : 119 – 42 . Google Scholar OpenURL Placeholder Text WorldCat Müller T , Thiße R, Braun S et al. (M)VOC and composting facilities Part 1: (M)VOC emissions from municipal biowaste and plant refuse . Environ Sci Pollution Res . 2004 ; 11 : 91 – 7 . Google Scholar OpenURL Placeholder Text WorldCat Naznin HA , Kimura M, Miyazawa M et al. Analysis of volatile organic compounds emitted by plant growth-promoting fungus Phoma sp GS8-3 for growth promotion effects on tobacco . Microbes Environ . 2013 ; 28 : 42 – 9 . Google Scholar OpenURL Placeholder Text WorldCat Nealson KH , Platt T, Hastings JW. Cellular control of the synthesis and activity of the bacterial luminescent system . J Bacteriol . 1970 ; 104 : 313 – 22 . Google Scholar OpenURL Placeholder Text WorldCat Nickerson KW , Atkin AL, Hornby JM. Quorum sensing in dimorphic fungi: farnesol and beyond . Appl Environ Microbiol . 2006 ; 72 : 3805 – 13 . Google Scholar OpenURL Placeholder Text WorldCat Ohshima S , Sato Y, Fujimura R et al. Mycoavidus cysteinexigens gen. nov., sp. nov., an endohyphal bacterium isolated from a soil isolate of the fungus Mortierella elongata . Int J Syst Evol Microbiol . 2016 ; 66 : 2052 – 7 . Google Scholar OpenURL Placeholder Text WorldCat Padder SA , Prasad R, Shah AH. Quorum sensing: a less known mode of communication among fungi . Microbiol Res . 2018 ; 210 : 51 – 8 . Google Scholar OpenURL Placeholder Text WorldCat Palkova Z , Janderova B, Gabriel J et al. Ammonia mediates communication between yeast colonies . Nature . 1997 ; 390 : 532 – 6 . Google Scholar OpenURL Placeholder Text WorldCat Papaleo MC , Fondi M, Maida I et al. Sponge-associated microbial Antarctic communities exhibiting antimicrobial activity against Burkholderia cepacia complex bacteria . Biotechnol Adv . 2012 ; 30 : 272 – 93 . Google Scholar OpenURL Placeholder Text WorldCat Papaleo MC , Romoli R, Bartolucci G et al. Bioactive volatile organic compounds from Antarctic (sponges) bacteria . New Biotechnol . 2013 ; 30 : 824 – 38 . Google Scholar OpenURL Placeholder Text WorldCat Pauliuc I , Botǎu D. Antibacterial activity of Pleurotus ostreatus gemmotherapic extract . J Hort Biotechnol . 2013 ; 17 : 242 – 5 . Google Scholar OpenURL Placeholder Text WorldCat Penuelas J , Asensio D, Tholl D et al. Biogenic volatile emissions from the soil . Plant Cell Environ . 2014 ; 37 : 1866 – 91 . Google Scholar OpenURL Placeholder Text WorldCat Perrin E , Maggini V, Maida I et al. Antimicrobial activity of six essential oils against Burkholderia cepacia complex: insights into mechanism(s) of action . Future Microbiol . 2018 ; 13 : 59 – 67 . Google Scholar OpenURL Placeholder Text WorldCat Pesavento G , Maggini V, Maida I et al. Essential oil from Origanum vulgare completely inhibits the growth of multidrug-resistant cystic fibrosis pathogens . Nat Prod Commun . 2016 ; 11 : 861 – 4 . Google Scholar OpenURL Placeholder Text WorldCat Piechulla B , Lemfack MC, Kai M. Effects of discrete bioactive microbial volatiles on plants and fungi . Plant Cell Environ . 2017 ; 40 : 2042 – 67 . Google Scholar OpenURL Placeholder Text WorldCat Pineda A , Soler R, Weldegergis BT et al. Nonpathogenic rhizobacteria interfere with the attraction of parasitoids to aphid-induced plant volatiles via jasmonic acid signalling . Plant Cell Environ . 2013 ; 36 : 393 – 404 . Google Scholar OpenURL Placeholder Text WorldCat Presta L , Bosi E, Fondi M et al. Phenotypic and genomic characterization of the antimicrobial producer Rheinheimera sp. EpRS3 isolated from the medicinal plant Echinacea purpurea: insights into its biotechnological relevance . Res Microbiol . 2017 ; 168 : 293 – 305 . Google Scholar OpenURL Placeholder Text WorldCat Raina S , Odell M, Keshavarz T. Quorum sensing as a method for improving sclerotiorin production in Penicillium sclerotiorum . J Biotechnol . 2010 ; 148 : 91 – 8 . Google Scholar OpenURL Placeholder Text WorldCat Ray S , Britschgi M, Herbert C et al. Classification and prediction of clinical Alzheimer's diagnosis based on plasma signaling proteins . Nat Med . 2007 ; 13 : 1359 – 62 . Google Scholar OpenURL Placeholder Text WorldCat Rodriguez RJ , White JF Jr, Arnold AE et al. Fungal endophytes: diversity and functional roles . New Phytol . 2009 ; 182 : 314 – 30 . Google Scholar OpenURL Placeholder Text WorldCat Rohm B , Scherlach K, Möbius N et al. Toxin production by bacterial endosymbionts of a Rhizopus microsporus strain used for tempe/sufu processing . Int J Food Microbiol . 2010 ; 136 : 368 – 71 . Google Scholar OpenURL Placeholder Text WorldCat Roychoudhry S , Del Bianco M, Kieffer M et al. Auxin controls gravitropic setpoint angle in higher plant lateral branches . Curr Biol . 2013 ; 23 : 1497 – 504 . Google Scholar OpenURL Placeholder Text WorldCat Schmidt R , Cordovez V, de Boer W et al. Volatile affairs in microbial interactions . ISME J . 2015 ; 9 : 2329 – 35 . Google Scholar OpenURL Placeholder Text WorldCat Schmidt R , Etalo DW, de Jager V et al. Microbial small talk: volatiles in fungal-bacterial interactions . Front Microbiol . 2016 ; 6 : 1495 . Google Scholar OpenURL Placeholder Text WorldCat Schmidt R , Jager V, Zühlke D et al. Fungal volatile compounds induce production of the secondary metabolite Sodorifen in Serratia plymuthica PRI-2CP . Sci Rep . 2017 ; 7 : 862 . Google Scholar OpenURL Placeholder Text WorldCat Schulz-Bohm K , Gerards S, Hundscheid M et al. Calling from distance: attraction of soil bacteria by plant root volatiles . ISME J . 2018 ; 12 : 1252 – 62 . Google Scholar OpenURL Placeholder Text WorldCat Schulz-Bohm K , Martín-Sánchez L, Garbeva P. Microbial Volatiles: small molecules with an important role in intra- and inter-kingdom interactions . Frontiers in Microbiology . 2017 ; 8 : 2484 . Google Scholar OpenURL Placeholder Text WorldCat Schüssler A , Kluge M. Geosiphon pyriforme, an endocytosymbiosis between fungus and cyanobacteria, and its meaning as a model system for arbuscular mycorrhizal research . In: Fungal associations . Berlin Heidelberg, Germany : Springer , 2011 , 151 – 61 . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Shaffer JP , Sarmiento C, Zalamea PC et al. Diversity, specificity, and phylogenetic relationships of endohyphal bacteria in fungi that inhabit tropical seeds and leaves . Front Ecol Evol . 2016 ; 4 : 116 . Google Scholar OpenURL Placeholder Text WorldCat Simard SW , Perry DA, Jones MD et al. Net transfer of carbon between ectomycorrhizal tree species in the field . Nature . 1997 ; 388 : 579 – 82 . Google Scholar OpenURL Placeholder Text WorldCat Sonnichsen R , Keller R. Methodische Grundlagen zur Identifizierung der flüchtigen organischen Stoffwechselprodukte von Schimmelpilzen mittels GC-MSD und Thermodesorption ± Schriftenreihe des Institutes für Medizinische Mikrobiologie und Hygiene der Medizinischen Universität Lübeck , In: Keller R (eds.), Lübeck : Heft 1 , 1997 , 161 – 92 . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Splivallo R , Bossi S, Maffei M et al. Discrimination of truffle fruiting body versus mycelial aromas by stir bar sorptive extraction . Phytochemistry . 2007 ; 68 : 2584 – 98 . Google Scholar OpenURL Placeholder Text WorldCat Splivallo R , Deveau A, Valdez N et al. Bacteria associated with truffle-fruiting bodies contribute to truffle aroma . Environ Microbiol . 2011 ; 81 : 2647 – 60 . Google Scholar OpenURL Placeholder Text WorldCat Splivallo R , Ebeler SE. Sulfur volatiles of microbial origin are key contributors to human-sensed truffle aroma . Appl Microbiol Biotechnol . 2015 ; 99 : 2583 – 92 . Google Scholar OpenURL Placeholder Text WorldCat Stefanini I . Yeast-insect associations: it takes guts . Yeast . 2018 ; 35 : 315 – 30 . Google Scholar OpenURL Placeholder Text WorldCat Sun X , Bonfante P, Tang M. Effect of volatiles versus exudates released by germinating spores of Gigaspora margarita on lateral root formation . Plant Physiol Biochem . 2015 ; 97 : 1 – 10 . Google Scholar OpenURL Placeholder Text WorldCat Tagu D , Lapeyrie F, Martin F. The ectomycorrhizal symbiosis: genetics and development . Plant Soil . 2002 ; 244 : 97 – 105 . Google Scholar OpenURL Placeholder Text WorldCat Tarkka M , Sarniguet A, Frey-Klett P. Inter-kingdom encounters: recent advances in molecular bacterium-fungus interactions . Curr Genet . 2009 ; 55 : 233 – 43 . Google Scholar OpenURL Placeholder Text WorldCat Taylor DL , Bruns D. Independent, specialized invasions of ectomycorrhizal mutualism by two non photosynthetic orchids . Proc Natl Acad Sci . 1997 ; 94 : 4510 – 5 . Google Scholar OpenURL Placeholder Text WorldCat Thorn RM , Greenman J. Microbial volatile compounds in health and disease conditions . J Breath Res . 2012 ; 6 : 024001 . Google Scholar OpenURL Placeholder Text WorldCat Tyc O , Song CX, Dickschat JS et al. The ecological role of volatile and soluble secondary metabolites produced by soil bacteria . Trends Microbiol . 2017 ; 25 : 280 – 92 . Google Scholar OpenURL Placeholder Text WorldCat Tyc O , Wolf AB, Garbeva P. The effect of phylogenetically different Bacteria on the fitness of Pseudomonas fluorescens in sand microcosms . PLoS One . 2015 ; 10 : e0119838 . Google Scholar OpenURL Placeholder Text WorldCat Tylka GL , Hussey RS, Roncadori RW. Axenic germination of vesicular-arbuscular mycorrhizal fungi: effect of selected Streptomyces species . Phytopathology . 1991 ; 81 : 754 – 9 . Google Scholar OpenURL Placeholder Text WorldCat Uehling J , Gryganskyi A, Hameed K et al. Comparative genomics of Mortierella elongata and its bacterial endosymbiont Mycoavidus cysteinexigens . Environ Microbiol . 2017 ; 19 : 2964 – 83 . Google Scholar OpenURL Placeholder Text WorldCat Vannini C , Carpentieri A, Salvioli A et al. An interdomain network: the endobacterium of a mycorrhizal fungus promotes antioxidative responses in both fungal and plant hosts . New Phytol . 2016 ; 211 : 265 – 75 . Google Scholar OpenURL Placeholder Text WorldCat Wang Y , Sun S, Zhu W et al. Strigolactone/MAX2-induced degradation of brassinosteroid transcriptional effector BES1 regulates shoot branching . Dev Cell . 2013 ; 27 : 681 – 8 . Google Scholar OpenURL Placeholder Text WorldCat Weise T , Kai M, Gummesson A et al. Volatile organic compounds produced by the phytopathogenic bacterium Xanthomonas campestris pv Vesicatoria . Beilstein J Org Chem . 2012 ; 8 : 579 – 96 . Google Scholar OpenURL Placeholder Text WorldCat Wenke K , Weise T, Warnke R et al. Bacterial volatiles mediating information between bacteria and plants . In: Witzany G (ed.) Biocommunication, signaling and communication in plants . Berlin, Heidelberg : Springer Verlag , 2012 , 327 – 48 . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Wessen B , Strom G, Palmgren U et al. Analysis of microbial volatile organic compounds . In: Flanagan B, Samson RA, Miller JD (eds.) Microorganisms in Home and Indoor Work Environments . London, UK : Taylor and Francis , 2001 , 267 – 74 . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Wongsuk T , Pumeesat P, Luplertlop N. Fungal quorum sensing molecules: role in fungal morphogenesis and pathogenicity . J Basic Microbiol . 2016 ; 56 : 440 – 7 . Google Scholar OpenURL Placeholder Text WorldCat Wurzenberger M , Grosch W. Stereochemistry of the cleavage of the 10-hydroperoxide isomer of linoleic acid to 1-octen-3-ol by a hydroperoxide lyase from mushrooms (Psalliota bispora) . Biochim Biophys Acta Lipids Lipid Metabol . 1984 ; 795 : 163 – 5 . Google Scholar OpenURL Placeholder Text WorldCat Zeringue HJ , Mccormick SP. Relationships between cotton leaf-derived volatiles and growth of Aspergillus flavus . J Am Oil Chem Soc . 1989 ; 66 : 581 – 5 . Google Scholar OpenURL Placeholder Text WorldCat Zhao LJ , Yang XN, Li XY et al. Antifungal, insecticidal and herbicidal properties of volatile components from Paenibacillus polymyxa Strain BMP-11 . Agric Sci China . 2011 ; 10 : 728 – 36 . Google Scholar OpenURL Placeholder Text WorldCat Zou CS , Mo MH, Gu YQ et al. Possible contribution of volatile-producing bacteria in soil fungistasis . Soil Biol Biochem . 2007 ; 39 : 2371 – 9 . Google Scholar OpenURL Placeholder Text WorldCat © The Author(s) 2021. Published by Oxford University Press on behalf of FEMS. This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model)
TI - Volatile organic compounds: from figurants to leading actors in fungal symbiosis
JO - FEMS Microbiology Ecology
DO - 10.1093/femsec/fiab067
DA - 2021-05-17
UR - https://www.deepdyve.com/lp/oxford-university-press/volatile-organic-compounds-from-figurants-to-leading-actors-in-fungal-e3Wz55PznM
VL - 97
IS - 5
DP - DeepDyve
ER -