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Mean (±SE) CO 2 emission of F. pratensis × L. perenne roots (n = 15). Student's t-test, **P = 0.01. For abbreviations, see Fig. 2
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Plants emit specific blends of volatile organic compounds (VOCs) that serve as multitrophic, multifunctional signals. Fungi colonizing aboveground (AG) or belowground (BG) plant structures can modify VOC patterns, thereby altering the information content for AG insects. Whether AG microbes affect the emission of root volatiles and thus influence so...
Citations
... General and specialized metabolism pathways exhibited pronounced differences between endophyte-infected and endophyte-free roots under A-N (Fig. 4), mirroring the accumulation of various organic acids, amino acids, and fatty acids reported by Hou et al. (49). Other metabolomic studies reveal Epichloë endophytes can modulate host stress resilience, growth, and soil insect distributions by altering root exudate composition and metabolic pathways (55,56). ...
The clavicipitaceous fungus Epichloë gansuensis forms symbiotic associations with drunken horse grass (Achnatherum inebrians), providing biotic and abiotic stress protection to its host. However, it is unclear how E. gansuensis affects the assembly of host plant-associated bacterial communities after ammonium nitrogen (NH4⁺-N) treatment. We examined the shoot- and root-associated bacterial microbiota and root metabolites of A. inebrians when infected (I) or uninfected (F) with E. gansuensis endophyte. The results showed more pronounced NH4⁺-N-induced microbial and metabolic changes in the endophyte-infected plants compared to the endophyte-free plants. E. gansuensis significantly altered bacterial community composition and β-diversity in shoots and roots and increased bacterial α-diversity under NH4⁺-N treatment. The relative abundance of 117 and 157 root metabolites significantly changed with E. gansuensis infection under water and NH4⁺-N treatment compared to endophyte-free plants. Root bacterial community composition was significantly related to the abundance of the top 30 metabolites [variable importance in the projection (VIP) > 2 and VIP > 3] contributing to differences between I and F plants, especially alkaloids. The correlation network between root microbiome and metabolites was complex. Microorganisms in the Proteobacteria and Firmicutes phyla were significantly associated with the R00693 metabolic reaction of cysteine and methionine metabolism. Co-metabolism network analysis revealed common metabolites between host plants and microorganisms.
IMPORTANCE
Our results suggest that the effect of endophyte infection is sensitive to nitrogen availability. Endophyte symbiosis altered the composition of shoot and root bacterial communities, increasing bacterial diversity. There was also a change in the class and relative abundance of metabolites. We found a complex co-occurrence network between root microorganisms and metabolites, with some metabolites shared between the host plant and its microbiome. The precise ecological function of the metabolites produced in response to endophyte infection remains unknown. However, some of these compounds may facilitate plant-microbe symbiosis by increasing the uptake of beneficial soil bacteria into plant tissues. Overall, these findings advance our understanding of the interactions between the microbiome, metabolome, and endophyte symbiosis in grasses. The results provide critical insight into the mechanisms by which the plant microbiome responds to nutrient stress in the presence of fungal endophytes.
... In the majority of studies, the alkaloids produced by grass endophyte have been detected in the above-ground tissues of host plants, such as shoots, leaves, and even seeds [30]. One study revealed that alkaloids are also present in the soil [69]. An in vitro experiment conducted on the native grass Bromus setifolius revealed that exudates of Epichloë species and endophyte-infected plants improved planta yield and also increased the mycelium length of AMF Gigaspora rosea by 100-200%, suggesting that Epichloë exudates enhance plant growth and yields, particularly through enhancing AMF development [70]. ...
In nature, plants frequently experience concurrent colonization with arbuscular mycorrhizal fungi (AMF) and grass endophytes (Epichloë). These two fungi assist in mineral uptake and stress tolerance by the host. Despite the abundance of recent studies exploring the individual functions of these fungi in diverse ecosystems, research on the effects of the interaction between these two symbiotic fungi on the host, particularly in agricultural production and ecological conservation. This review provides an overview of the current knowledge regarding the interaction between AMF and grass endophytes and their synergistic effects on host plants in response to abiotic and biotic stress, while also outlining prospects for future research in this field. This knowledge not only enhances our comprehension of complex interaction effects between the two fungi, but also facilitates the optimal utilization of fungal resources, contributing to ecological construction and higher agricultural production.
... 2,3 Nowadays, several reports highlight the role of volatile organic compounds (VOCs) as a key factor in the fungal ecological interactions with other fungi, bacteria, and plants. 4 These VOCs are known to regulate growth in spores and seeds, 5 modify signaling for herbivore deterrence, 6 pathogen inhibition, 7 among other functions. The production of VOCs by fungi is influenced by numerous factors, including environmental conditions. ...
Fungi exhibit a wide range of ecological guilds, but those that live within the inner tissues of plants (also known as endophytes) are particularly relevant due to the benefits they sometimes provide to their hosts, such as herbivory deterrence, disease protection, and growth promotion. Recently, endophytes have gained interest as potential biocontrol agents against crop pathogens, for example, coffee plants (Coffea arabica). Published results from research performed in our laboratory showed that endophytic fungi isolated from wild Rubiaceae plants were effective in reducing the effects of the American leaf spot of coffee (Mycena citricolor). One of these isolates (GU11N) from the plant Randia grandifolia was identified as Daldinia eschscholtzii (Xylariales). Its antagonism mechanisms, effects, and chemistry against M. citricolor were investigated by analyzing its volatile profile alone and in the presence of the pathogen in contactless and dual culture assays. The experimental design involved direct sampling of agar plugs in vials for headspace (HS) and headspace solid-phase microextraction (HS-SPME) gas chromatography-mass spectrometry (GC-MS) analysis. Additionally, we used ultrahigh-performance liquid chromatography coupled to high-resolution mass spectrometry (UHPLC-HRMS/MS) to identify nonvolatile compounds from organic extracts of the mycelia involved in the interaction. Results showed that more volatile compounds were identified using HS-SPME (39 components) than those by the HS technique (13 components), sharing only 12 compounds. Statistical tests suggest that D. eschscholtzii inhibited the growth of M. citricolor through the release of VOCs containing a combination of 1,8-dimethoxynapththalene and terpene compounds affecting M. citricolor pseudopilei. The damaging effects of 1,8-dimethoxynaphthalene were corroborated in an in vitro test against M. citricolor pseudopilei; scanning electron microscopy (SEM) photographs confirmed structural damage. After analyzing the UHPLC-HRMS/MS data, a predominance of fatty acid derivatives was found among the putatively identified compounds. However, a considerable proportion of features (37.3%) remained unannotated. In conclusion, our study suggests that D. eschscholtzii has potential as a biocontrol agent against M. citricolor and that 1,8-dimethoxynaphthalene contributes to the observed damage to the pathogen's reproductive structures.
... Several studies of root-feeding arthropod responses to chemical cues from plant roots used bioassay methods designed to mimic the soil environment (e.g., Hibbard and Bjostad, 1989;Horton and Landolt, 2002;Johnson et al., 2004;Weissteiner et al., 2012;Kojima et al., 2014;Rostas et al., 2015;Liu et al., 2016;Wu and Duncan, 2020). This likely reflects the economic importance of root-feeding arthropods and the necessity to grow plants in soil to conduct meaningful experiments. ...
Chemical signaling underpins behavioral interactions among organisms in the soil. Understanding chemical communication in the soil requires a paradigm shift in methodology and perspectives compared to aboveground ecosystems because olfaction and gustation, accepted modalities of chemosensation aboveground, may not accurately represent chemical communication in the soil. To fully understand chemical communication in the soil, it is essential to consider how soil properties, such as moisture, pH, and adsorption, affect the transport and perception of semiochemicals. De-anthropomorphizing the study of chemosensation can avoid potential biases, particularly in soil systems, where distinctions between olfaction and gustation are confounded by the heterogeneity of the soil environment and its effects on the mobility of chemical signals. In this perspective, we first explore how soil heterogeneity confounds the dichotomy between olfaction and gustation with hypothetical but ecologically relevant examples. Then we examine how anthropomorphic biases in aboveground chemical ecology have influenced soil chemical ecology. Our examples and discussion are prepared primarily in reference to soil arthropods. We conclude by discussing seven future research directions and outstanding questions. The soil is a premier example of a system where investigators should avoid anthropomorphisms when studying behavioral and chemical ecology. Research in soil chemical ecology should further efforts towards developing a unified view of chemosensation that could apply to all environments where chemical communication occurs.
... Root herbivory can also modify aboveground emission of volatiles, ultimately affecting the behavior and biology of aboveground organisms and vice versa Rasmann and Turlings 2007;Soler et al. 2007Soler et al. , 2009Erb et al. 2011;Ye et al. 2022). Thereby, the host plant can serve as a communication channel between the above-and belowground environments (Soler et al. 2009;Rostás et al. 2015). ...
According to the theory of optimal foraging and preference–performance hypothesis, herbivores usually select plant hosts that benefit themselves or their offspring. We investigated the hypothesis that gravid females of the cucurbit beetle Diabrotica speciosa use volatiles derived from non-infested maize plants and herbivore-infested plants under attack by their conspecific immatures and adults in selecting a host for oviposition. The response of D. speciosa females to volatiles was quantified for the following treatments: (i) non-infested plants; (ii) plants infested by larvae (root-infested); (iii) plants infested by adults (leaf-infested); and (iv) plants infested by larvae and adults (leaf + root-infested). We also assessed if females were able to identify conditions of competition and host adequacy for offspring by means of chemical cues emitted by these plants. The results indicated that the presence of D. speciosa conspecifics on maize plants triggered the emission of volatiles, which influenced host selection for oviposition. Gravid females avoided both plants infested by larvae and plants infested by larvae and adults. Leaf-infested plants did not affect the host-selection behavior of females. Weight gain was higher in larvae kept on non-infested and leaf-infested plants than on root-infested or root + leaf-infested plants, indicating that female preference is related to its offspring performance.
Graphical Abstract
Synthesis of the effects of volatile organic compounds (VOCs) produced by uninfested, leaf-infested, root-infested and leaf+root-infested corn plants on the host-choice behavior of adults and performance of Diabrotica speciosa larvae
... In conclusion, this work shows that VOCs emission induced by a type of beneficial interaction between the plant and an asexual fungus depends on whether the presence of other symbioses is contemplated. Although it is known that the presence of symbiotic microorganisms -like AMF or foliar endophytes -modifies the emission of VOCs in their host plants (Sharifi et al. 2018), the emission can be induced (Yue et al. 2001;Schausberger et al. 2012;Ballhorn et al. 2013;Li et al. 2014;Fiorenza et al. 2021) or reduced (Babikova et al. 2014;Rostás et al. 2015) depending on the microorganism-plant pair that we observed. In the light of our results, we propose that the variability can be explained, at least in part, also because of the simultaneous presence of other beneficial symbioses that were not considered before. ...
Most cool season grasses are commonly associated with asexual endophytes and arbuscular mycorrhizal fungi (AMF). These two symbionts are known to provide different benefits to the host plant through altering its phenotype when they are present. In isolation, either of them can affect the volatile organic compounds (VOCs) emitted by the host grass, but their interactive influences on this trait are unknown. We hypothesized that changes in host grasses VOCs profile induced by the presence of asexual endophytes within aerial tissues, depend on whether these plants are also colonized by AMF. We designed a factorial greenhouse experiment, in which we identified and quantified VOCs emitted by Lolium multiflorum plants with contrasting levels of infection with the endophyte Epichloë occultans (low < 5% and high > 95%), growing in pots with sterilized soil that could be inoculated or not with AMF. Results showed that total VOCs emission in plants with high infection levels of E. occultans doubled the emission of plants with low levels of the endophyte, but only in plants previously inoculated with AMF. The green leaf volatile Z3-Hexenyl acetate dominated the blend. Its emission was three times higher in plants with high level of association with both types of symbionts compared to plants with high level of AMF but low level of endophyte. We found a similar trend for the monoterpene β-ocimene. Our results point out the importance of considering the contribution of different types of symbionts when studying the interaction of plants with their natural enemies or the benefits provided to the host in different ecological contexts.
... Other studies on host grasses with an Epichloë endophyte also focused on metabolites in general, rather than just alkaloids. A study found that Neotyphodium uncinatum (=Epichloë uncinata) endophytes in host plants may affect soil insect distribution by altering the presence of root volatiles that affect insect behavior (75). Epichloë coenophiala in tall fescue can affect root exudate composition, including lipids, carbohydrates. ...
... Impact factors on the microbes of seeds and glumes. Soil possesses high microbial diversity, and this directly and indirectly influences seed microbes (75,76). A recent study showed that many soil bacteria could reach the leaves and flowers of Arabidopsis thaliana (77). ...
The seed-borne microbiota and seed metabolites of the grass Achnatherum inebrians, either host to Epichloë gansuensis (endophyte infected [EI]) or endophyte free (EF), were investigated. This study determined the microbial communities both within the seed (endophytic) and on the seed surface (epiphytic) and of the protective glumes by using Illumina sequencing technology. Epichloë gansuensis decreased the richness of the seed-borne microbiota except for the epiphytic fungi of glumes and also decreased the diversity of seed-borne microbiota. In addition, metabolites of seeds and glumes were detected using liquid chromatography-mass spectrometry (LC-MS). Unlike with the seeds of EF plants, the presence of E. gansuensis resulted in significant changes in the content of 108 seed and 31 glume metabolites. A total of 319 significant correlations occurred between seed-borne microbiota and seed metabolites; these correlations comprised 163 (147 bacterial and 16 fungal) positive correlations and 156 (136 bacterial and 20 fungal) negative correlations. Meanwhile, there were 42 significant correlations between glume microbiota and metabolites; these correlations comprised 28 positive (10 bacterial and 18 fungal) and 14 negative (9 bacterial and 5 fungal) correlations. The presence of E. gansuensis endophyte altered the communities and diversities of seed-borne microbes and altered the composition and content of seed metabolites, and there were many close and complex relationships between microbes and metabolites. IMPORTANCE The present study was to investigate seed-borne microbiota and seed metabolites in Achnatherum inebrians using high-throughput sequencing and LC-MS technology. Epichloë gansuensis decreased the richness of the seed-borne microbiota except for the epiphytic fungi of glumes and also decreased the diversity of seed-borne microbiota. Compared with endophyte-free plants, the content of 108 seed and 31 glume metabolites of endophyte-infected plants was significantly changed. There were 319 significant correlations between seed-borne microbiota and seed metabolites and 42 significant correlations between glume microbiota and metabolites.
... The endophytic fungus Neotyphodium uncinatum, which colonizes the aerial parts of the grass hybrid Festuca pratensis × Lolium perenne, can reduce the emission of root volatiles. 95 Effects of benecial microbes might be mediated by the increased N availability and other resources needed for volatile biosynthesis, 96 but also by the modulation of defense signaling. 97 In the case of insect symbionts, the presence of the endosymbiont Hamiltonella defensa in pea aphid (Acyrthosiphon pisum) has been shown to compromise plant indirect defenses (i.e., parasitoid attraction) by altering volatile emission upon aphid feeding. ...
Covering: up to November 2022Plants shape terrestrial ecosystems through physical and chemical interactions. Plant-derived volatile organic compounds in particular influence the behavior and performance of other organisms. In this review, we discuss how vegetative plant volatiles derived from leaves, stems and roots are produced and released into the environment, how their production and release is modified by abiotic and biotic factors, and how they influence other organisms. Vegetative plant volatiles are derived from different biosynthesis and degradation pathways and are released via distinct routes. Both biosynthesis and release are regulated by other organisms as well as abiotic factors. In turn, vegetative plant volatiles modify the physiology and the behavior of a wide range of organisms, from microbes to mammals. Several concepts and frameworks can help to explain and predict the evolution and ecology of vegetative plant volatile emission patterns of specific pathways: multifunctionality of specialized metabolites, chemical communication displays and the information arms race, and volatile physiochemistry. We discuss how these frameworks can be leveraged to understand the evolution and expression patterns of vegetative plant volatiles. The multifaceted roles of vegetative plant volatiles provide fertile grounds to understand ecosystem dynamics and harness their power for sustainable agriculture.
... Changes in the rhizosphere microbial community can be associated with plant mechanisms of nutrient acquisition (e.g., phosphorus solubilization), and recruiting beneficial microbes while reducing the presence and action of the negative ones; the so-called cry for help (Rizaludin et al. 2021). In particular, plant symbioses with Epichloë species have been found to alter root exudates and VOCs (Guo et al. 2015;Rostás et al. 2015;Van Hecke et al. 2005) and consequently, the microorganisms in the rhizosphere . Compared to non-symbiotic plants, different strains of E. coenophiala changed the total biomass and relative abundance of fungi in the rhizosphere of tall fescue (Rojas et al. 2016). ...
The immense importance of microbial symbioses with plants, animals, and other eukaryotes is meeting with ever increasing awareness and interest. Heritable symbionts—those transmitted directly from hosting parents to hosting progeny—are particularly intimate associations with profound ecological, evolutionary, and applied consequences. However, heritable symbioses also tend to be inconspicuous and are often understudied. Heritable fungal symbionts of plants, which we call seed endophytes, have been discovered and rediscovered in a few grass species (family Poaceae) starting well over a century ago, but have been intensively researched only in the last 45 years since their ability to produce antimammalian alkaloids was revealed to cause major toxicoses to livestock. The characterization of those fungal Epichloë species has been followed gradually by documentation of other seed endophytes with bioactive alkaloids, such as those found in locoweeds (family Fabaceae) and morning glories (family Convolvulaceae). As the known species diversity of seed endophytes and their hosts has expanded, so too has our knowledge of their alkaloid diversity, defenses against invertebrates, positive and negative effects on host plants, effects on pathogens and beneficial symbionts (e.g., mycorrhizal fungi), protection from abiotic stresses such as drought, and cascading population, community, and ecosystem consequences. Recent studies have even revealed endophyte contributions to plant diversity, including an Epichloë gene apparently transferred to a host grass in which it confers disease resistance. Here we review the current knowledge of seed-endophyte symbioses with emphasis on their phylogenetic, genetic, and functional diversity.
... Previous meta-analysis and experiment cases showed that the presence of Epichloë endophytes stimulated root exudation [8] and altered the composition of root exudates of the host grass [20,21]. For example, Epichloë-infected grass roots release more carbon (in the form of phenolic compounds and amines) into the rhizosphere through root exudation and volatiles than non-infected grasses [20,27]. Some secondary metabolites (such as lipids, flavonoids, and phenolic compounds) could regulate the presymbiotic phase of plant-AMF symbiosis [28,29] at the start of the connection of AMF initial mycelium with plant roots [30]. ...
Many grasses are simultaneously symbiotic with Epichloë fungal endophytes and arbuscular mycorrhizal fungi (AMF). Epichloë endophytes are a group of filamentous fungi that colonize and grow within aerial plant tissues, such as leaves and stems. Infection and hyphal growth of Epichloë endophytes confer fitness advantages to the host plants. In addition to producing fungal alkaloids and altering host metabolic/genetic profiles, it is proven that symbiosis of plants with root/foliar endophytes affects the plant–soil relationship. We propose that the Epichloë presence/infection results in variations of soil and root AMF through allelopathic effects. We performed a meta-analysis that integrated the allelopathic effects of Epichloë endophytes on grass–AMF development. In the pre-symbiotic phase of grass–AMF symbiosis, root exudation from Epichloë-infected plants positively affected AMF growth, whereas the shoot exudates of Epichloë-infected plants inhibited AMF growth. In the symbiotic phase of grass–AMF symbiosis, the Epichloë infection was found to reduce root mycorrhizal colonization in plants. No pattern in the response of soil AMF to Epichloë presence was found. This study should improve our understanding of the impact of Epichloë endophytes on belowground microbial symbionts within the same host plant. Grass–Epichloë–AMF symbiosis may become an important model for studying above–belowground interactions.
