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Review

The Interaction between Arbuscular Mycorrhizal Fungi (AMF) and Grass Endophyte (Epichloë) on Host Plants: A Review

by
Youlei Shen
1,2,3,4,5 and
Tingyu Duan
1,2,3,4,5,*
1
State Key Laboratory of Herbage Improvement and Grassland Agro-Ecosystems, Lanzhou University, Lanzhou 730020, China
2
College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou 730020, China
3
Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Affairs, Lanzhou 730020, China
4
Engineering Research Center of Grassland Industry, Ministry of Education, Lanzhou 730020, China
5
Gansu Tech Innovation Center of Western China Grassland Industry, Lanzhou 730020, China
*
Author to whom correspondence should be addressed.
J. Fungi 2024, 10(3), 174; https://doi.org/10.3390/jof10030174
Submission received: 1 December 2023 / Revised: 12 February 2024 / Accepted: 19 February 2024 / Published: 26 February 2024
(This article belongs to the Special Issue Fungal Endophytes of Grasses)
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Abstract

:
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.

1. Introduction

Natural ecosystems comprise numerous microbial communities. Plants can form symbiotic associations with diverse fungi [1,2,3]. Cold-season grasses in grasslands can establish symbiotic relationships with arbuscular mycorrhizal fungi (AMF) of the phylum Glomeromycota and grass endophytes of the genus Epichloë [4,5,6].
Arbuscular mycorrhizal fungi constitute diverse and significant microorganisms in soils and various ecosystems, even those in adverse conditions [7,8,9,10]. Over 80% of terrestrial plants roots form symbiotic relationships with AMF [11]. AMF increases the root absorption surface area, thereby enhancing the uptake of nutrients such as nitrogen and phosphorus, promoting photosynthesis, and regulating photosynthetic product distribution, ultimately improving plant growth [12,13,14,15]. Furthermore, AMF promotes the host plant’s resistance to adverse environmental stressors, including drought, heavy metals, microplastics, and biotic stresses such as pathogens and herbivory insects [16,17,18,19,20,21,22,23,24,25]. In reciprocation, plants supply AMF with the necessary carbon sources for their growth and survival [26,27]. The enduring relationship between AMF and host plants, established over an extended period of evolution, is characterized as a well-established symbiotic association [15,28,29].
Grass endophytes are fungi of the genus Epichloë that form symbiotic relationships strictly with certain species of C3 grasses in the Pooideae subfamily, including numerous forage and turf grasses [30]. The endophytic colonization by the grass endophyte occurs within the intercellular spaces of the host’s sheaths and leaves and is passed to the host’s progeny through vertical transmission, seed dispersal, or both [31]. The host plant nourishes and creates a conducive environment for the endophyte’s growth. In return, the endophyte enhances the host’s resilience to both biotic and abiotic stressors, improving the nutrient absorption efficiency of the host plant [32,33,34,35]. Most cold-season grasses can establish symbiotic relationships with endophytic fungi belonging to the genus Epichloë.
AMF and grass endophytes are important below-ground and above-ground microorganisms that often colonize the same host plants, forming complex AMF-Epichloë-plant associations called tripartite interactions. Understanding how plant-microbiome and microbe-microbe interactions occur has been the subject of increasing research interest [36,37,38,39,40]; particularly, the symbiosis patterns of multiple microorganisms, including both above-ground and below-ground microorganisms, and the ecological mechanisms underlying host plant-microbial community interactions. Such research can provide valuable insights for future microbial and genetic engineering. Knowledge of the interaction between AMF, grass endophytes, and their host plants in ecosystems remains scanty. To shed light on this topic, we present a review of recent articles on the interactions between AMF and grass endophytes. Our aims were to (1) provide an overview of how grass endophytes and AMF promote stress tolerance in host plants; (2) describe the mechanism of interaction between these two symbionts with host plants; and (3) identify priority areas for future research on the tripartite interaction between AMF, grass endophytes, and host plants.

2. Effect of Grass Endophyte on Arbuscular Mycorrhiza

2.1. Effect of Grass Endophyte on Mycorrhizal Colonization

Grasses are usually simultaneously colonized by grass endophytes and AMF, and these two symbiotic fungi inhabit both the above-ground and below-ground parts of the host plant [30,41]. Numerous studies have investigated how grass endophytes affect the rate of mycorrhizal colonization. The specific outcome is contingent upon the grass species and the particular combination of grass endophyte and mycorrhizal fungi involved, as detailed in Table 1. The main grass species studied in regard to the above association include Lolium perenne, Lolium multiflorum, Achnatherum sibiricum, Schedonorus arundinaceus, Bromus auleticus, Leymus chinensis, Festuca paniculata, Elymus hystrix, and Poa bonariensis (Lam.) Kunth.
The presence of grass endophytes can cause several effects on mycorrhizal colonization rates, ranging from negative [42,43] to positive [44], or neutral [45]. An initial investigation into the effect of grass endophytes on mycorrhizal colonization by Chuchou et al. [42] revealed that the concurrent infection of Festuca arundinacea with Epichloë coenophiala and Funneliformis mosseae decreased the root colonization rates by 41.2%. Other researchers have similarly found that infection of Lolium perenne with Epichloë festucae var. lolii reduced colonization by mycorrhizal Claroideoglomus etunicatum [43]. However, the opposite outcome was observed when host plants were exposed to stress. For example, Epichloë endophytes increased mycorrhizal colonization by 85.21% when Lolium perenne was infected with the pathogenic fungi Bipolaris sorokiniana [44]. Nevertheless, numerous studies indicate that grass endophytes do not affect mycorrhizal colonization [45]. Thus, we assumed that the effect of grass endophytes on mycorrhizal colonization rates depends on specific interaction outcomes among the mycorrhizal fungi, grass endophytes, host plant species, and environmental conditions. Further studies on the interactions between different AMF and grass endophytes, and the underlying mechanisms, are needed.
A few studies have investigated how mycorrhizal fungi affect the effect of grass endophytes on host plants [46,47,48]. For instance, Liu et al. (2011) found a negative correlation between the concentration of grass endophyte and mycorrhizal fungi colonization rate. The reduction in mycorrhizal fungi colonization positively correlated with soil P content and was dependent on the ryegrass cultivar and the grass endophyte strains [46]. Mack and Rudgers (2007) found that AMF had no effect on grass endophyte density [47], while Liu et al. (2020) found AMF could have a positive, negative, or no impact on grass endophyte concentration; the increased impact mostly occurred with Glomus intraradices individuals and its mix with other AMF [48]. Liu et al. (2011) further found that the inhibition of AMF by grass endophytes is linked with the reduction of alkaloids in the leaf blade and pseudostems of perennial ryegrass by Glomus [46]. More research is required to clarify the mutual benefits of the symbiotic association between grass endophytes and AMF colonization and the function of alkaloids, plant defenses, and signal molecules in these associations.
Table 1. Effect of grass endophytes on the mycorrhizal root colonization of host plants.
Table 1. Effect of grass endophytes on the mycorrhizal root colonization of host plants.
Host PlantsGrass EndophyteAM FungiStudy SiteInfluenceMechanismReferences
Agrostis capillarisEpichloë sp.Live soil inoculationFieldNo impact./[45]
Bromus auleticusEpichloë pampeana; Epichloë tembladeraeLive soil inoculationField+18% at 6 months after fertilization.Genotype of host plants, and the exudate of different profile of compounds.[49]
Bromus auleticusEpichloë sp.Living vertisol soilField+21%~33%, +29% of abuscules and vesicles of the other neighbor grasses.Grass-Epichloë association generate a soil environment through secreting root exudates.[5]
Bromus auleticusEpichloë pampeanaLiving field soilGreenhouse+19%~43%.The soil types of (agriculture soil and non-agriculture soil).[50]
Elymus hystrixEpichloë elymiGlomus claroideum,
Glomus mosseae		Greenhouse−13%~19% when inoculated with G. claroideum but +15% with the G. mosseae.Identity of the AMF species.[51]
Festuca arundinacea Schreb.Acremonium coenophiulum
(Epichloë coenophialum)		Funneliformis mosseaeGreenhouse−41.2%.The toxic metabolites transferred to the root.[42]
Hordeum comosumEpichloë tembladeraeLiving grassland soilField+8%.Differentiation of the plant niche and the external precipitation.[52]
Leymus chinensisEpichloë bromicolaLiving grassland soilField+15%.Endophyte affected the soil properties.[53]
Lolium arundinaceumEpichloë coenophialumFunneliformis mosseae;
Claroideoglomus etunicatum		Greenhouse−1.1% in saline-alkali stress of colonization rate of F. mosseae;
+30.7%~38% colonization rate of C. etunicatum;
+8%~32.2% colonization rate of the mixture of FM and CE.		Species of AMF and environmental conditions.[54]
Lolium perenne
(Fenneama and AberDart)		Neotyphodium lolii
(Epichloë festucae var. lolii)		Glomus intraradices;
Glomus mosseae		Greenhouse−72.7% of Fenneama varieties, but had no effect on AberDart.Species and specific of AMF and host plant.[46]
Lolium perenneEpichloë festucae var. loliiClaroideoglomus etunicatumGreenhouseMuch lower AMF colonization rate at 70% soil water contents.Soil water contents.[55]
Schedonorus arundinaceusEpichloë coenophialaLiving pasture soilField−53.6%.Competition of C of Epichloë and AMF from host plant.[56]
Schedonorus phoenixNeotyphodium coenophialum
(Epichloë coenophialum)		live soil inoculumGreenhouse−50.2%./[47]

2.2. Mechanisms Underlying the Effect of Grass Endophyte on Mycorrhizal Colonization

The mechanism through which Epichloë endophytes affect the colonization pattern of AM fungi in the roots is not well understood. As mentioned in the preceding section, environmental conditions, external stresses (biotic or abiotic stresses), host plant species, and AMF species, among other factors, affect the colonization of arbuscular mycorrhizal fungi [57,58,59,60]. Hence, the mechanisms by which root-symbiont interactions are affected by Epichloë are very complex and require an in-depth investigation.
The effect of grass endophytes on the colonization of AM fungi can be categorized into direct and indirect modes. Compared to AMF, Epichloë endophytes have better spatial advantages. Epichloë is seed-borne and mainly exists in the above-ground stems and leaves of plants [30]. When AMF and grass endophytes concurrently colonize a host plant, both fungi rely on plant-derived carbon sources for growth. However, due to their time and spatial advantage within the above-ground stems and leaves, endophytes are granted preferential access to photosynthetic carbohydrates, potentially diminishing the availability of these products for AMF utilization. This resource competition may consequently inhibit the infection of AM fungi [47].
In AMF-grass endophyte-plants systems, Epichloë increases shoot/root phosphorus concentrations and net photosynthesis rates [44,52,55,61,62]. In this association, AMF provides a substantial amount of phosphorus-containing compounds to host plants in exchange for photosynthetic products [63,64]. In soil nutrient deficiency cases, the host’s reliance on AM fungi may decrease. Moreover, it has been observed that the rhizosphere of plants colonized with grass endophytes exhibits higher aggregate stability compared with those not colonized [65]. Thereby, we hypothesize that the variations in plant growth and nutrient availability resulting from colonization with grass endophytes can indirectly impact the diversity of the microbial community, altering mycorrhizal colonization [66].
Compounds exuded from the roots of plants greatly promote root mycorrhizal colonization, and identifying those compounds is essential for unraveling the mechanisms of root mycorrhizal colonization. Grass endophytes protect their host plants by producing secondary metabolites, including Loline, Peramine, Ergot, and Lolitrems [67], which can deter herbivore and insect feeding, providing direct plant defense [68]. 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]. Furthermore, the association between Bromus catharticus and grass endophytes enhanced the mycorrhizal colonization of Lolium multiflorum, Schedonorus arundinaceus, and Bromus catharticus [71]. Colonization of Lolium perenne by mycorrhizal fungi reduced the abundance of grass endophytes and the secretion of anti-herbivore-associated alkaloids peramine and lolitrem B [46]. However, so far, the mechanism by which alkaloids produced by grass endophytes impact AMF development is not understood.

3. Effect of Concurrent Colonization of AMF and Grass Endophyte on Host Plant

3.1. Effect of Co-Colonization of AMF and Grass Endophyte on Host Plant Growth

The effects of AMF and grass endophyte interaction on plant growth are diverse, ranging from negative [54] to positive [55] and neutral [56] (Table 2). According to a greenhouse experiment, colonization with Epichloë festucae var. lolii and AMF Claroideoglomus etunicatum significantly increased the total biomass and dry weight of Lolium perenne [55]. Furthermore, concurrent colonization with the two fungi increased the plant’s P uptake and physiological indexes such as dry biomass, hormones, and root length. These findings suggest that the interaction between grass endophyte and AMF can positively affect plant growth. Liu et al. found a positive correlation between the shoot P concentrations and the abundance of AMF and grass endophyte [72]. Additionally, Wezowicz et al. reported that inoculating Verbascum lychnitis with both fungi significantly increased the abundance of Photosystem II protein and plant chlorophyll concentration [73].
Although grass endophytes and AMF can promote various growth parameters in plants, it should be noted that the beneficial effects of these two fungi are not always obvious. For example, simultaneous colonization with grass endophytes and AMF had no effect on the growth of Bromus auleticus [5]. Furthermore, Neotyphodium occultans (Epichloë occultans) and AMF did not improve the performance or nutrient content of Lolium multiflorum [74]. Surprisingly, when Lolium arundinaceum was infected with Epichloë coenophialum, inoculation with the AMF Funneliformis mosseae negatively impacted shoot and root biomass, while the presence of the AMF Claroideoglomus etunicatum significantly promoted plant growth [54]. This means that AM fungi can diminish the benefits of grass endophytes. These results indicate that in the tripartite interactions between grass endophytes, AMF, and host species, the benefits depend on the interactions between the AMF and host species, and the grass endophyte and AMF species. By gaining a deeper understanding of the mechanisms behind these effects, it may be possible to optimize the use of fungi to increase plant yield and improve quality.
Table 2. The effects of co-infection of arbuscular mycorrhizal fungi and grass endophyte on host plant.
Table 2. The effects of co-infection of arbuscular mycorrhizal fungi and grass endophyte on host plant.
PlantsGrass EndophyteAM FungiStudy SiteResultsReferences
Lolium perenneEpichloë festucae var. loliiClaroideoglomus etunicatumGreenhouse+44.53%, 30.27%, and 28.47% of dry weight in soil moisture conditions of 30%, 50%, and 70%.[55]
Leymus chinensisEpichloë bromicolaGlomus etunicatum
Glomus intraradices		Greenhouse+73.21% P absorption.[48]
Lolium arundinaceumEpichloë coenophialumClaroideoglomus etunicatum;
Funneliformis mosseae		GreenhouseInoculated with F. mosseae alone, −41.79% and −68.82% of shoot biomass and root biomass, had no impact in salt-alkali stress.[54]
Achnatherum sibiricumEpichloë sibiricaGlomus mosseae;
Glomus etunicatum		GreenhouseGreater competitive ability.[4]
Achnatherum sibiricumEpichloë sibiricaGlomus mosseae;
Glomus etunicatum		Greenhouse+12.5% and 10.55% of the total phenolic content when inoculated with GM and GE respectively.[75]
Lolium multiflorumNeotyphodium occultans
(Epichloë occultans)		Glomus mosseae;
Glomus caledonium;
Glomus fasciculatum		GreenhouseNo impact.[74]
Lolium perenneEpichloë typhina; Neotyphodium lolii
(Epichloë festucae var. lolii)		Sclerocystis sp. GreenhouseHigher shoot-root biomass ration.[76]
Lolium perenneEpichloë festucae var. loliiClaroideoglomus etunicatumGreenhouseHighest values of SOD, POD, the total P content, and the total dry weight.[43]

3.2. Effect of Simultaneous Colonization with AMF and Grass Endophyte on Biotic Resistance of Host Plant

Throughout the growth and development process, plants are subjected to different stresses from biotic and abiotic factors, and even experience both types of stress simultaneously. Previous studies have primarily focused on the effects of either grass endophytes or AMF on the host’s resistance to biotic or abiotic stress. Because AMF and grass endophytes simultaneously colonize the same host plant, it is essential to explore the combined effect of these fungi on the host plant’s resistance to stress. We believe that this interaction has the potential to significantly influence plant health and productivity.
To date, a few researchers have demonstrated that AMF-grass endophyte-plant associations can enhance host plant tolerance to various stressors (Table 3). A greenhouse-based study demonstrated that inoculating ryegrass with both Claroideoglomus etunicatum and Epichloë festucae var. lolii reduced the severity of leaf spot caused by B. sorokiniana, and the levels of malondialdehyde and hydrogen peroxide were lower [43]. Similarly, a related study revealed a decrease in the abundance of pathogens due to the increased production of total phenols in Achnatherum sibiricum induced by the colonization of Glomus etunicatum and Epichloë sibirica [77].
Grass endophytes confer prominent advantages to host plants, such as alkaloid production, induction of expression of anti-herbivore feeding genes, and alteration of volatile substance composition, which discourages feeding by herbivores [78]. The enhancement of plant resistance by AMF is undeniable [25,79]. However, studies on the interactions between grass endophytes and AMF and the resulting repulsion of herbivores and other biological stresses by the host plant remain scanty.
At present, only a few studies have shown that the interactions between AMF and grass endophytes have reduced the feeding of some plants by herbivores. In 2002, Mark et al. used perennial ryegrass (Lolium perenne cv. “Express”) to investigate the effect of the interaction between Glomus mosseae and Neotyphodium lolii (Epichloë festucae var. lolii) on the noctuid Phlogophora meticulosa [80]. The study revealed that the presence of grass endophytes and mycorrhizal fungi cumulatively decreased the survival of second to fifth-instar larvae, and the effect was greater when the plant had adequate phosphorus. Additionally, there was a negative correlation between the interaction between the two fungi and feeding by insects. Notably, grass endophytes amplified the relative larval feeding rate while concurrently diminishing the insect’s food conversion efficiency. Conversely, mycorrhizal fungi had no obvious effect on the feeding behavior.
Pathogens and pest insects usually infect or feed on the same host plants. Currently, only a few studies have investigated the interplay between AMF and grass endophytes in relation to simultaneous infestation with pathogens and insects. Our understanding of the influence of plant defenses on symbiotic fungal endophytes is limited.
Table 3. Results of co-infection of arbuscular mycorrhizal fungi and grass endophyte on plant resistance to abiotic and biotic stress.
Table 3. Results of co-infection of arbuscular mycorrhizal fungi and grass endophyte on plant resistance to abiotic and biotic stress.
PlantsGrass EndophyteAM FungiStressResultsReferences
Lolium perenneEpichloë festucae var. loliiClaroideoglomus etunicatumWaterEnhanced uptake of phosphorus (P), elevated photosynthetic activity, and the accumulation of osmoregulatory compounds.[55]
Lolium arundinaceumEpichloëcoenophialumClaroideoglomus etunicatum;
Funneliformis mosseae		Saline-alkaliCE significantly enhanced saline-alkali resistance by increasing potassium (K+) accumulation and reducing sodium (Na+) concentration, whereas resistance was reduced following inoculation with FM.[54]
Leymus chinensisEpichloë bromicolaFunneliformis mosseaeDroughtAMF enhanced the drought resistance of EF plants, yet had no significant effect on the drought resistance of EI plants.[81]
Lolium perenne cv. “Express”Neotyphodium lolii
(Epichloë festucae var. lolii)		Glomus mosseaePestMycorrhizal and endophyte interaction was observed in third-instar larvae regarding survivorship.[80]
Lolium perenneEpichloë festucae var. loliiClaroideoglomus etunicatumPathogenSuppressed the occurrence of leaf spot by increasing the levels of chemical substances and the plant defensive enzymes.[44]
Lolium perenneEpichloë festucae var. loliiClaroideoglomus etunicatumPathogenDecrease disease incidence by 10.93%, elevated plant defensive activity levels but reduced concentrations of MDA and H2O2.[43]
Achnatherum sibiricumEpichloë sibiricaGlomus etunicatumPathogenIncreased production of total phenols of plants, and thus decreased the abundance of pathogen.[77]

3.3. Effects of Simultaneous Colonization of AMF and Grass Endophyte on Host Plant Resistance to Abiotic Stress

Compared with research on biotic stress, research on the impact of simultaneous inoculation with AMF and grass endophytes on abiotic stressors, such as drought, saline-alkali, and water, is more well-established. Simultaneous colonization with AMF and grass endophytes was found to significantly increase the concentration of soluble sugar and peroxidase activity under 30% soil water content [55]. Lolium arundinaceum was inoculated with Epichloë coenophialum and either Claroideoglomus etunicatum or Funneliformis mossea under different saline-alkali contents. Interestingly, inoculation with Epichloë coenophialum and Claroideoglomus etunicatum increased the resistance of the host, compared to plants inoculated with the AMF Funneliformis mossea and Epichloë coenophialum [54]. Benefits of grass endophytes may be diminished or weakened by inoculation with Funneliformis mossea, and this has been reported in many studies. For instance, inoculating Leymus chinensis with Epichloë bromicola and Funneliformis mosseae weakened its drought stress tolerance [81].
Indeed, the effect of infection with two symbionts on plant resistance is a complex and multifaceted phenomenon, and the interaction between different factors needs to be further explored. While numerous studies have investigated the benefits and drawbacks of individual above-ground or below-ground microorganisms on host plants, only a few studies have investigated the tripartite interactions between grass endophytes, AM fungi, and host plants.
Dual symbiotic fungal-plant interactions have been found to increase plant biomass, enhance the activity of defense enzymes, increase nutrient uptake rate, and modify net photosynthetic rate. For instance, a study conducted on Lolium perenne found that the grass endophyte Epichloë and AMF Claroideoglomus etunicatum increased the total dry weight and phosphorus (P) content of the plant and induced higher activity of defense enzymes, including peroxidase (POD), polyphenol oxidase (PPO), and catalase (CAT) and lower concentrations of malondialdehyde (MDA) under drought stress conditions [55]. The enhanced performance of host plants under drought stress could be attributed to the altered activity of anti-stress enzymes. In addition, co-infection with Epichloë and Claroideoglomus etunicatum enhanced the saline-alkali stress tolerance of Lolium arundinaceum by increasing K+ concentration and nutrient uptake while decreasing Na+ concentration [54]. These studies provide evidence that AMF and grass endophytes can simultaneously modulate the physiological responses of host plants to external stress (Figure 1).
Furthermore, the interaction between AMF and grass endophytes can alleviate stress in plants by modulating the response of secondary metabolites and their proportions and regulating the expression of genes related to stress. These factors can affect the growth and development of host plants, as well as their tolerance to stress. One research study demonstrated that co-inoculation with AMF Claroideoglomus etunicatum and grass endophyte Epichloë festucae var. lolii reduced the disease index caused by B. sorokiniana in ryegrass by increasing the accumulation of soluble protein [43]. Under certain conditions, combining AMF and grass endophytes may not always result in synergistic effects on the host plants. For instance, under water stress, mycorrhizal inoculation significantly increased proline content by 15% and total phenolic concentration by 18% in endophyte-free Leymus chinensis, but the treatment had no significant effects on endophyte-infected plants [81].
Only a few studies have investigated the mechanisms of interactions between AMF and grass endophytes and plants at the molecular level. Our research group conducted a study of AMF-grass endophyte-pathogen interactions in perennial ryegrass using RNA-seq analysis [82]. We found unexpected results that showed that both AMF and grass endophytes significantly increased the expression of genes related to the regulation of SOD, POD, PPO, and CAT activity. Interestingly, the number of genes whose expression was up-regulated induced by the interaction between AMF and grass endophytes was higher than infection with two fungi. Moreover, this interaction also induced terpenoid backbone biosynthesis, biotin metabolism, aldehyde metabolism, and the expression of proteins involved in plant-pathogen interactions. The up-regulation of SOD, PPO, POD, CAT, and SA-related genes also occurred. Furthermore, it also induced the expression of 11 pathogenesis-related genes (PRGs), and the Heat Shock Factor (HSF) significantly enhanced the disease resistance of plants (Figure 1). Future research should focus on this area to better understand events under multiple symbioses.

3.4. Effect of Simultaneous Colonization with AMF and Grass Endophyte on Plant Competitive Ability

Grass endophytes and AMF could positively impact the competitive ability of host plants [83,84,85]. Specifically, some studies have reported that grass endophytes mostly positively affect inter-specific or intra-specific competition and induce plant community shifts by promoting host growth, including increasing the number of tillers and enhancing root and shoot biomass or the production of allelopathic substances. However, only a few studies have investigated the effect of dual infections on the performance of plant competition. A study showed that the presence of both grass endophytes and AM fungi can enhance the growth performance and inter-specific competition ability of Achnatherum sibiricum, leading to changes in the plant community structure that promotes the coexistence of dominant species (Stipa grandis) and subordinate species (Achnatherum sibiricum) [4]. So far, the mechanisms underlying the effects of mycorrhizal inoculation and endophytes on altering plant community structure are poorly understood.

4. Conclusions and Future Perspectives

In recent years, plant-microbe interactions have gained considerable attention, and exploration of the interactions between plants and plant microbiomes is an important area for elucidating the mechanisms of interspecies interactions. Increasing evidence suggests that both above-ground and below-ground microbes provide various functions for their host plants, such as promoting growth, enhancing nutrient uptake, improving abiotic stress tolerance, and increasing biotic resistance and tolerance, including disease resistance [86,87,88,89,90]. In AM-Epichloë-plant associations, AMF and Epichloë endophyte increase nutrient uptake, enhance photosynthesis and increase phytohormone levels, enhance plant defense, alter the production of volatile compounds, modulate plant resistance related gene expression, and increase plant resistance to biotic and abiotic stress (Figure 1). The interactions between above-ground and below-ground microorganisms and their impact on plants have long been recognized as a crucial frontier for comprehending fundamental biochemical and ecological processes in both agricultural and natural ecosystems. In addition, the current limitations of research methods and data analysis models have impeded our understanding of these interactions and have hindered our ability to effectively leverage microbial resources to enhance productivity and ecological value. Herein, we highlighted the interactions between above-ground microorganisms (grass endophytes) and below-ground microorganisms (AMF) and how multiple symbionts shape the performance of host plants under different stress conditions. We propose that the species, and whether they occur alone or simultaneously with other symbiotic fungi, are the most important factors that determine whether they confer beneficial, harmful, or neutral effects to the host plants. The effects of grass endophytes and AMF on host plant growth and development depend on the degree of host signals and environmental stress. Simultaneous infection with fungi plays a critical role in determining host plant performance, and the relative importance and functional effects of these symbiotic processes vary depending on plant species, developmental stage, and microbial community.
Despite recent advances significantly expanding our understanding of the symbiotic processes and functions of grass endophytes and AM fungi, our knowledge of the molecular mechanisms underlying simultaneous infections and their effect on plant defenses and growth remains limited. Moreover, the practical applications of multiple plant-microbe interactions in sustainable agriculture and the protection of ecology still lag behind. For example, some critical research areas remain largely unexplored: (1) How do Epichloë-colonized plants recruit AMF at different growth stages? (2) Which kinds of keystone functional genes in the Epichloë-AMF-plant system enhance host resistance to biotic and abiotic stresses? (3) Can, and how do, the Epichloë-AMF-plant systems recruit beneficial microbes with desired functions under various environmental conditions? (4) How do Epichloë-AMF-plant complexes and their microbiomes interact and co-evolve in response to different agricultural management practices and global climatic changes over a long time? (5) How do grass endophytes and AMF affect the movement and utilization of nutrients in the above-ground and below-ground plant parts? (6) What is the function and role of AMF-Epichloë-plant symbionts on carbon fixation, species diversity, community stability, and the productivity of the ecosystem? Answering these questions can contribute to our knowledge of the underlying mechanisms of Epichloë-AMF-plants interactions and provide essential information for precisely harnessing beneficial microbiomes, including developing agricultural sustainability.

Author Contributions

Y.S. and T.D. wrote and edited the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

Funding for this research was provided by the China Modern Agriculture Research System (CARS-22 Green Manure).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

All applicable data are published and referenced in the paper.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Ramirez, K.S.; Geisen, S.; Morrien, E.; Snoek, B.L.; van der Putten, W.H. Network Analyses Can Advance Above-Belowground Ecology. Trends Plant Sci. 2018, 23, 759–768. [Google Scholar] [CrossRef]
  2. Bais, H.P.; Weir, T.L.; Perry, L.G.; Gilroy, S.; Vivanco, J.M. The role of root exudates in rhizosphere interations with plants and other organisms. Annu. Rev. Plant Biol. 2006, 57, 233–266. [Google Scholar] [CrossRef]
  3. Wardle, D.A.; Bardgett, R.D.; Klironomos, J.N.; Setala, H.; van der Putten, W.H.; Wall, D.H. Ecological linkages between aboveground and belowground biota. Science 2004, 304, 1629–1633. [Google Scholar] [CrossRef]
  4. Zhou, Y.; Li, X.; Gao, Y.; Liu, H.; Gao, Y.-B.; van der Heijden, M.G.A.; Ren, A.-Z. Plant endophytes and arbuscular mycorrhizal fungi alter plant competition. Funct. Ecol. 2018, 32, 1168–1179. [Google Scholar] [CrossRef]
  5. Vignale, M.V.; Iannone, L.J.; Novas, V. Epichloë endophytes of a wild grass promote mycorrhizal colonization of neighbor grasses. Fungal Ecol. 2020, 45, 100916. [Google Scholar] [CrossRef]
  6. Novas, M.V.; Cabral, D.; Godeas, A.M. Interaction between grass endophytes and mycorrhizas in Bromus setifolius from Patagonia, Argentina. Symbiosis 2005, 40, 23–30. [Google Scholar]
  7. Smith, S.E.; Read, D. Mycorrhizal symbiosis; Academic Press: Cambridge, UK, 2008. [Google Scholar]
  8. Akiyama, K.; Matsuzaki, K.; Hayashi, H. Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 2005, 435, 824–827. [Google Scholar] [CrossRef]
  9. Bernardo, L.; Carletti, P.; Badeck, F.W.; Rizza, F.; Morcia, C.; Ghizzoni, R.; Rouphael, Y.; Colla, G.; Terzi, V.; Lucini, L. Metabolomic responses triggered by arbuscular mycorrhiza enhance tolerance to water stress in wheat cultivars. Plant Physiol. Biochem. 2019, 137, 203–212. [Google Scholar] [CrossRef]
  10. Estrada, B.; Aroca, R.; Maathuis, F.J.M.; Miguel Barea, J.; Manuel Ruiz-Lozano, J. Arbuscular mycorrhizal fungi native from a Mediterranean saline area enhance maize tolerance to salinity through improved ion homeostasis. Plant Cell Environ. 2013, 36, 1771–1782. [Google Scholar] [CrossRef]
  11. Harrison, M.J. Cellular programs for arbuscular mycorrhizal symbiosis. Curr. Opin. Plant Biol. 2012, 15, 691–698. [Google Scholar] [CrossRef]
  12. Shi, Z.Y.; Zhang, J.C.; Lu, S.C.; Li, Y.; Wang, F.Y. Arbuscular Mycorrhizal Fungi Improve the Performance of Sweet Sorghum Grown in a Mo-Contaminated Soil. J. Fungi 2020, 6, 44. [Google Scholar] [CrossRef]
  13. Boutasknit, A.; Baslam, M.; Ait-El-Mokhtar, M.; Anli, M.; Ben-Laouane, R.; Douira, A.; El Modafar, C.; Mitsui, T.; Wahbi, S.; Meddich, A. Arbuscular Mycorrhizal Fungi Mediate Drought Tolerance and Recovery in Two Contrasting Carob (Ceratonia siliqua L.) Ecotypes by Regulating Stomatal, Water Relations, and (In)Organic Adjustments. Plants 2020, 9, 80. [Google Scholar] [CrossRef]
  14. Yang, Y.R.; Song, Y.Y.; Scheller, H.V.; Ghosh, A.; Ban, Y.H.; Chen, H.; Tang, M. Community structure of arbuscular mycorrhizal fungi associated with Robinia pseudoacacia in uncontaminated and heavy metal contaminated soils. Soil Biol. Biochem. 2015, 86, 146–158. [Google Scholar] [CrossRef]
  15. Johnson, N.C.; Graham, J.H.; Smith, F.A. Functioning of mycorrhizal associations along the mutualism-parasitism continuum. New Phytol. 1997, 135, 575–586. [Google Scholar] [CrossRef]
  16. Li, Y.; Wang, X.; Chen, X.; Lu, J.; Jin, Z.; Li, J. Functions of arbuscular mycorrhizal fungi in regulating endangered species Heptacodium miconioides growth and drought stress tolerance. Plant Cell Rep. 2023, 42, 1967–1986. [Google Scholar] [CrossRef]
  17. Han, Y.; Xu, T.; Chen, H.; Tang, M. Sugar metabolism and 14-3-3 protein genes expression induced by arbuscular mycorrhizal fungi and phosphorus addition to response drought stress in Populus cathayana. J. Plant Physiol. 2023, 288, 154075. [Google Scholar] [CrossRef]
  18. Xing, S.; Shen, Q.; Ji, C.; You, L.; Li, J.; Wang, M.; Yang, G.; Hao, Z.; Zhang, X.; Chen, B. Arbuscular mycorrhizal symbiosis alleviates arsenic phytotoxicity in flooded Iris tectorum Maxim. dependent on arsenic exposure levels. Environ. Pollut. 2024, 340, 122841. [Google Scholar] [CrossRef]
  19. Chen, H.; Zhang, X.; Wang, H.; Xing, S.; Yin, R.; Fu, W.; Rillig, M.C.; Chen, B.; Zhu, Y. Arbuscular Mycorrhizal Fungi Can Inhibit the Allocation of Microplastics from Crop Roots to Aboveground Edible Parts. J. Agric. Food Chem. 2023, 71, 18323–18332. [Google Scholar] [CrossRef]
  20. Israel, A.; Langrand, J.; Fontaine, J.; Sahraoui, A.L.H. Significance of Arbuscular Mycorrhizal Fungi in Mitigating Abiotic Environmental Stress in Medicinal and Aromatic Plants: A Review. Foods 2022, 11, 2591. [Google Scholar] [CrossRef]
  21. Riaz, M.; Kamran, M.; Fang, Y.Z.; Wang, Q.Q.; Cao, H.Y.; Yang, G.L.; Deng, L.L.; Wang, Y.J.; Zhou, Y.Y.; Anastopoulos, I.; et al. Arbuscular mycorrhizal fungi-induced mitigation of heavy metal phytotoxicity in metal contaminated soils: A critical review. J. Hazard. Mater. 2021, 402, 123919. [Google Scholar] [CrossRef]
  22. Doubkova, P.; Suda, J.; Sudova, R. The symbiosis with arbuscular mycorrhizal fungi contributes to plant tolerance to serpentine edaphic stress. Soil Biol. Biochem. 2012, 44, 56–64. [Google Scholar] [CrossRef]
  23. Gao, Y.Z.; Li, Q.L.; Ling, W.T.; Zhu, X.Z. Arbuscular mycorrhizal phytoremediation of soils contaminated with phenanthrene and pyrene. J. Hazard. Mater. 2011, 185, 703–709. [Google Scholar] [CrossRef]
  24. Wang, D.; Pan, M.; Biere, A.; Ding, J. Arbuscular mycorrhizal fungi and belowground herbivores interact to determine plant productivity and performance of subsequently feeding conspecifics by changing plant metabolites. J. Pest Sci. 2023. [Google Scholar] [CrossRef]
  25. Liu, M.; Wang, H.; Lin, Z.; Ke, J.; Zhang, P.; Zhang, F.; Ru, D.; Zhang, L.; Xiao, Y.; Liu, X. Arbuscular mycorrhizal fungi inhibit necrotrophic, but not biotrophic, aboveground plant pathogens: A meta-analysis and experimental study. New Phytol. 2023, 241, 1308–1320. [Google Scholar] [CrossRef]
  26. Jiang, Y.; Wang, W.; Xie, Q.; Liu, N.; Liu, L.; Wang, D.; Zhang, X.; Yang, C.; Chen, X.; Tang, D.; et al. Plants transfer lipids to sustain colonization by mutualistic mycorrhizal and parasitic fungi. Science 2017, 356, 1172–1175. [Google Scholar] [CrossRef]
  27. Wang, W.; Shi, J.; Xie, Q.; Jiang, Y.; Yu, N.; Wang, E. Nutrient Exchange and Regulation in Arbuscular Mycorrhizal Symbiosis. Mol. Plant 2017, 10, 1147–1158. [Google Scholar] [CrossRef]
  28. Lambers, H.; Mougel, C.; Jaillard, B.; Hinsinger, P. Plant-microbe-soil interactions in the rhizosphere: An evolutionary perspective. Plant Soil 2009, 321, 83–115. [Google Scholar] [CrossRef]
  29. Shi, J.; Wang, X.; Wang, E. Mycorrhizal Symbiosis in Plant Growth and Stress Adaptation: From Genes to Ecosystems. Annu. Rev. Plant Biol. 2023, 74, 569–607. [Google Scholar] [CrossRef]
  30. Bastias, D.A.; Alejandra Martinez-Ghersa, M.; Ballare, C.L.; Gundel, P.E. Epichloë Fungal Endophytes and Plant Defenses: Not Just Alkaloids. Trends Plant Sci. 2017, 22, 939–948. [Google Scholar] [CrossRef]
  31. Zhang, W.; Card, S.D.; Mace, W.J.; Christensen, M.J.; McGill, C.R.; Matthew, C. Defining the pathways of symbiotic Epichloë colonization in grass embryos with confocal microscopy. Mycologia 2017, 109, 153–161. [Google Scholar] [CrossRef]
  32. Xia, C.; Zhang, X.; Christensen, M.J.; Nan, Z.; Li, C. Epichloë endophyte affects the ability of powdery mildew (Blumeria graminis) to colonise drunken horse grass (Achnatherum inebrians). Fungal Ecol. 2015, 16, 26–33. [Google Scholar] [CrossRef]
  33. Song, M.; Chai, Q.; Li, X.; Yao, X.; Li, C.; Christensen, M.J.; Nan, Z. An asexual Epichloë endophyte modifies the nutrient stoichiometry of wild barley (Hordeum brevisubulatum) under salt stress. Plant Soil 2015, 387, 153–165. [Google Scholar] [CrossRef]
  34. Ma, M.; Christensen, M.J.; Nan, Z. Effects of the endophyte Epichloë festucae var. lolii of perennial ryegrass (Lolium perenne) on indicators of oxidative stress from pathogenic fungi during seed germination and seedling growth. Eur. J. Plant Pathol. 2015, 141, 571–583. [Google Scholar] [CrossRef]
  35. Li, C.; Nan, Z.; Li, F. Biological and physiological characteristics of Neotyphodium gansuense symbiotic with Achnatherum inebrians. Microbiol. Res. 2008, 163, 431–440. [Google Scholar] [CrossRef]
  36. Geller, A.M.; Levy, A. “What I cannot create, I do not understand”: Elucidating microbe-microbe interactions to facilitate plant microbiome engineering. Curr. Opin. Microbiol. 2023, 72, 102283. [Google Scholar] [CrossRef]
  37. Ginnan, N.A.; De Anda, N.I.; Campos Freitas Vieira, F.; Rolshausen, P.E.; Roper, M.C. Microbial Turnover and Dispersal Events Occur in Synchrony with Plant Phenology in the Perennial Evergreen Tree Crop Citrus sinensis. MBio 2022, 13, e0034322. [Google Scholar] [CrossRef]
  38. Regalado, J.; Lundberg, D.S.; Deusch, O.; Kersten, S.; Karasov, T.; Poersch, K.; Shirsekar, G.; Weigel, D. Combining whole-genome shotgun sequencing and rRNA gene amplicon analyses to improve detection of microbe-microbe interaction networks in plant leaves. ISME J. 2020, 14, 2116–2130. [Google Scholar] [CrossRef]
  39. Dastogeer, K.M.G.; Tumpa, F.H.; Sultana, A.; Akter, M.A.; Chakraborty, A. Plant microbiome-an account of the factors that shape community composition and diversity. Curr. Plant Biol. 2020, 23, 100161. [Google Scholar] [CrossRef]
  40. Vorholt, J.A.; Vogel, C.; Carlstrom, C.I.; Mueller, D.B. Establishing Causality: Opportunities of Synthetic Communities for Plant Microbiome Research. Cell Host Microbe 2017, 22, 142–155. [Google Scholar] [CrossRef]
  41. Parniske, M. Arbuscular mycorrhiza: The mother of plant root endosymbioses. Nat. Rev. Microbiol. 2008, 6, 763–775. [Google Scholar] [CrossRef]
  42. Chuchou, M.; Guo, B.; An, Z.Q.; Hendrix, J.W.; Ferriss, R.S.; Siegel, M.R.; Dougherty, C.T.; Burrus, P.B. Suppression of mycprrhizal fungi in fescue by the Acremonium-Coenophialum endophyte. Soil Biol. Biochem. 1992, 24, 633–637. [Google Scholar] [CrossRef]
  43. Li, F.; Guo, Y.e.; Christensen, M.J.; Gao, P.; Li, Y.; Duan, T. An arbuscular mycorrhizal fungus and Epichloë festucae var. lolii reduce Bipolaris sorokiniana disease incidence and improve perennial ryegrass growth. Mycorrhiza 2018, 28, 159–169. [Google Scholar] [CrossRef]
  44. Guo, Y.; Gao, P.; Li, F.; Duan, T. Effects of AM fungi and grass endophytes on perennial ryegrass Bipolaris sorokiniana leaf spot disease under limited soil nutrients. Eur. J. Plant Pathol. 2019, 154, 659–671. [Google Scholar] [CrossRef]
  45. Vandegrift, R.; Roy, B.A.; Pfeifer-Meister, L.; Johnson, B.R.; Bridgham, S.D. The herbaceous landlord: Integrating the effects of symbiont consortia within a single host. PeerJ 2015, 3, e1379. [Google Scholar] [CrossRef]
  46. Liu, Q.; Parsons, A.J.; Xue, H.; Fraser, K.; Ryan, G.D.; Newman, J.A.; Rasmussen, S. Competition between foliar Neotyphodium lolii endophytes and mycorrhizal Glomus spp. fungi in Lolium perenne depends on resource supply and host carbohydrate content. Funct. Ecol. 2011, 25, 910–920. [Google Scholar] [CrossRef]
  47. Mack, K.M.L.; Rudgers, J.A. Balancing multiple mutualists: Asymmetric interactions among plants, arbuscular mycorrhizal fungi, and fungal endophytes. Oikos 2008, 117, 310–320. [Google Scholar] [CrossRef]
  48. Liu, H.; Wu, M.; Liu, J.; Qu, Y.; Gao, Y.; Ren, A. Tripartite Interactions Between Endophytic Fungi, Arbuscular Mycorrhizal Fungi, and Leymus chinensis. Microb. Ecol. 2020, 79, 98–109. [Google Scholar] [CrossRef]
  49. Victoria Vignale, M.; Iannone, L.J.; Daniela Pinget, A.; De Battista, J.P.; Victoria Novas, M. Effect of epichloë endophytes and soil fertilization on arbuscular mycorrhizal colonization of a wild grass. Plant Soil 2016, 405, 279–287. [Google Scholar] [CrossRef]
  50. Arrieta, A.M.; Iannone, L.J.; Scervino, J.M.; Vignale, M.V.; Novas, M.V. A foliar endophyte increases the diversity of phosphorus-solubilizing rhizospheric fungi and mycorrhizal colonization in the wild grass Bromus auleticus. Fungal Ecol. 2015, 17, 146–154. [Google Scholar] [CrossRef]
  51. Larimer, A.L.; Bever, J.D.; Clay, K. Consequences of simultaneous interactions of fungal endophytes and arbuscular mycorrhizal fungi with a shared host grass. Oikos 2012, 121, 2090–2096. [Google Scholar] [CrossRef]
  52. Casas, C.; Gundel, P.E.; Deliens, E.; Iannone, L.J.; Garcia Martinez, G.; Vignale, M.V.; Schnyder, H. Loss of fungal symbionts at the arid limit of the distribution range in a native Patagonian grass-Resource eco-physiological relations. Funct. Ecol. 2022, 36, 583–594. [Google Scholar] [CrossRef]
  53. Liu, H.; Wu, M.; Liu, J.; Gao, Y.; Ren, A. Endophyte infection influences arbuscular mycorrhizal fungi communities in rhizosphere soils of host as opposed to non-host grass. Eur. J. Soil Sci. 2021, 72, 995–1009. [Google Scholar] [CrossRef]
  54. Liu, H.; Tang, H.; Ni, X.; Zhang, Y.; Wang, Y. Interactive Effects of Epichloë Endophytes and Arbuscular Mycorrhizal Fungi on Saline-Alkali Stress Tolerance in Tall Fescue. Front. Microbiol. 2022, 13, 855890. [Google Scholar] [CrossRef]
  55. Li, F.; Deng, J.; Nzabanita, C.; Li, Y.; Duan, T. Growth and physiological responses of perennial ryegrass to an AMF and an Epichloë endophyte under different soil water contents. Symbiosis 2019, 79, 151–161. [Google Scholar] [CrossRef]
  56. Slaughter, L.C.; Nelson, J.A.; Carlisle, E.; Bourguignon, M.; Dinkins, R.D.; Phillips, T.D.; McCulley, R.L. Climate change and Epichloë coenophiala association modify belowground fungal symbioses of tall fescue host. Fungal Ecol. 2018, 31, 37–46. [Google Scholar] [CrossRef]
  57. Wang, X.Q.; Wang, Y.H.; Song, Y.B.; Dong, M. Formation and functions of arbuscular mycorrhizae in coastal wetland ecosystems: A review. Ecosyst. Health Sustain. 2022, 8, 2144465. [Google Scholar] [CrossRef]
  58. Qin, M.S.; Li, L.; Miranda, J.P.; Tang, Y.; Song, B.; Oosthuizen, M.K.; Wei, W.R. Experimental duration determines the effect of arbuscular mycorrhizal fungi on plant biomass in pot experiments: A meta-analysis. Front. Plant Sci. 2022, 13, 1024874. [Google Scholar] [CrossRef]
  59. Jongen, M.; Albadran, B.; Beyschlag, W.; Unger, S. Can arbuscular mycorrhizal fungi mitigate drought stress in annual pasture legumes? Plant Soil 2022, 472, 295–310. [Google Scholar] [CrossRef]
  60. Kalosa-Kenyon, E.; Slaughter, L.C.; Rudgers, J.A.; McCulley, R.L. Asexual Epichloë Endophytes Do Not Consistently Alter Arbuscular Mycorrhizal Fungi Colonization in Three Grasses. Am. Midl. Nat. 2018, 179, 157–165. [Google Scholar] [CrossRef]
  61. Zhu, Y.; Zhu, S.; Zhang, F.; Zhao, Z.; Christensen, M.J.J.; Nan, Z.; Zhang, X. Transcriptomic Analyses Reveals Molecular Regulation of Photosynthesis by Epichloë endophyte in Achnatherum inebrians under Blumeria graminis Infection. J. Fungi 2022, 8, 1201. [Google Scholar] [CrossRef]
  62. Li, X.; Zhou, Y.; Mace, W.; Qin, J.; Liu, H.; Chen, W.; Ren, A.; Gao, Y. Endophyte species influence the biomass production of the native grass Achnatherum sibiricum (L.) Keng under high nitrogen availability. Ecol. Evol. 2016, 6, 8595–8606. [Google Scholar] [CrossRef]
  63. Berruti, A.; Lumini, E.; Balestrini, R.; Bianciotto, V. Arbuscular Mycorrhizal Fungi as Natural Biofertilizers: Let’s Benefit from Past Successes. Front. Microbiol. 2016, 6, 1559. [Google Scholar] [CrossRef]
  64. Walder, F.; Niemann, H.; Natarajan, M.; Lehmann, M.F.; Boller, T.; Wiemken, A. Mycorrhizal Networks: Common Goods of Plants Shared under Unequal Terms of Trade. Plant Physiol. 2012, 159, 789–797. [Google Scholar] [CrossRef]
  65. Hosseini, F.; Mosaddeghi, M.R.; Hajabbasi, M.A.; Sabzalian, M.R. Influence of tall fescue endophyte infection on structural stability as quantified by high energy moisture characteristic in a range of soils. Geoderma 2015, 249, 87–99. [Google Scholar] [CrossRef]
  66. Zhong, R.; Zhang, L.; Zhang, X. Allelopathic Effects of Foliar Epichloë Endophytes on Belowground Arbuscular Mycorrhizal Fungi: A Meta-Analysis. Agriculture 2022, 12, 1768. [Google Scholar] [CrossRef]
  67. Bastias, D.A.; Alejandra Martinez-Ghersa, M.; Newman, J.A.; Card, S.D.; Mace, W.J.; Gundel, P.E. The plant hormone salicylic acid interacts with the mechanism of anti-herbivory conferred by fungal endophytes in grasses. Plant Cell Environ. 2018, 41, 395–405. [Google Scholar] [CrossRef]
  68. Song, Q.-Y.; Li, F.; Nan, Z.-B.; Coulter, J.A.; Wei, W.J. Do Epichloë Endophytes and Their Grass Symbiosis Only Produce Toxic Alkaloids to Insects and Livestock? J. Agric. Food Chem. 2020, 68, 1169–1185. [Google Scholar] [CrossRef]
  69. Michael, R.; Cripps, M.G.; Patrick, S. Aboveground endophyte affects root volatile emission and host plant selection of a belowground insect. Oecologia 2015, 177, 487–497. [Google Scholar]
  70. Victoria Vignale, M.; Iannone, L.J.; Martin Scervino, J.; Victoria Novas, M. Epichloë exudates promote in vitro and in vivo arbuscular mycorrhizal fungi development and plant growth. Plant Soil 2018, 422, 267–281. [Google Scholar] [CrossRef]
  71. Terlizzi, N.L.; Rodriguez, M.A.; Iannone, L.J.; Lanari, E.; Novas, M.V. Epichloë endophyte affects the root colonization pattern of belowground symbionts in a wild grass. Fungal Ecol. 2022, 57–58, 101143. [Google Scholar] [CrossRef]
  72. Liu, H.; Tang, H.; Ni, X.; Zhang, Y.; Wang, Y. Effects of the endophyte Epichloë coenophiala on the root microbial community and growth performance of tall fescue in different saline-alkali soils. Fungal Ecol. 2022, 57–58, 101159. [Google Scholar] [CrossRef]
  73. Wezowicz, K.; Rozpadek, P.; Turnau, K. Interactions of arbuscular mycorrhizal and endophytic fungi improve seedling survival and growth in post-mining waste. Mycorrhiza 2017, 27, 499–511. [Google Scholar] [CrossRef]
  74. Omacini, M.; Eggers, T.; Bonkowski, M.; Gange, A.C.; Jones, T.H. Leaf endophytes affect mycorrhizal status and growth of co-infected and neighbouring plants. Funct. Ecol. 2006, 20, 226–232. [Google Scholar] [CrossRef]
  75. Zhou, Y.; Li, X.; Qin, J.; Liu, H.; Chen, W.; Niu, Y.; Ren, A.; Gao, Y. Effects of simultaneous infections of endophytic fungi and arbuscular mycorrhizal fungi on the growth of their shared host grass Achnatherum sibiricum under varying N and P supply. Fungal Ecol. 2016, 20, 56–65. [Google Scholar] [CrossRef]
  76. Muller, J. Artificial infection by endophytes affects growth and mycorrhizal colonisation of Lolium perenne. Funct. Plant Biol. 2003, 30, 419–424. [Google Scholar] [CrossRef]
  77. Zhang, J.; Deng, Y.; Ge, X.; Shi, X.; Fan, X.; Dong, K.; Chen, L.; Zhao, N.; Gao, Y.; Ren, A. The beneficial effect of Epichloë endophytes on the growth of host grasses was affected by arbuscular mycorrhizal fungi, pathogenic fungi and nitrogen addition. Environ. Exp. Bot. 2022, 201, 104979. [Google Scholar] [CrossRef]
  78. Schardl, C.L.; Young, C.A.; Faulkner, J.R.; Florea, S.; Pan, J. Chemotypic diversity of epichloae, fungal symbionts of grasses. Fungal Ecol. 2012, 5, 331–344. [Google Scholar] [CrossRef]
  79. Li, Y.; Nan, Z.; Matthew, C.; Wang, Y.; Duan, T. Arbuscular mycorrhizal fungus changes alfalfa (Medicago sativa) metabolites in response to leaf spot (Phoma medicaginis) infection, with subsequent effects on pea aphid (Acyrthosiphon pisum) behavior. New Phytol. 2023, 239, 286–300. [Google Scholar] [CrossRef]
  80. Vicari, M.; Hatcher, P.E.; Ayres, P.G. Combined effect of foliar and mycorrhizal endophytes on an insect herbivore. Ecology 2002, 83, 2452–2464. [Google Scholar] [CrossRef]
  81. Liu, H.; Chen, W.; Wu, M.; Wu, R.; Zhou, Y.; Gao, Y.; Ren, A. Arbuscular mycorrhizal fungus inoculation reduces the drought-resistance advantage of endophyte-infected versus endophyte-free Leymus chinensis. Mycorrhiza 2017, 27, 791–799. [Google Scholar] [CrossRef] [PubMed]
  82. Deng, J. Mechanisms of Effects of Arbuscular Mycorrhizal Fungus and Grass Endophyte on Leaf Spot of Perennial Ryegrass (in Chinese). Master’s Dissertation, Lanzhou University, Lanzhou, China, 2021. [Google Scholar]
  83. Clay, K.; Marks, S.; Cheplick, G.P. Effects of insect herbivory and fungal endophyte infection on competitive interactions among grasses. Ecology 1993, 74, 1767–1777. [Google Scholar] [CrossRef]
  84. Muller, C.B.; Krauss, J. Symbiosis between grasses and asexual fungal endophytes. Curr. Opin. Plant Biol. 2005, 8, 450–456. [Google Scholar] [CrossRef] [PubMed]
  85. Averill, C.; Turner, B.L.; Finzi, A.C. Mycorrhiza-mediated competition between plants and decomposers drives soil carbon storage. Nature 2014, 505, 543–545. [Google Scholar] [CrossRef] [PubMed]
  86. Stringlis, I.A.; de Jonge, R.; Pieterse, C.M.J. The Age of Coumarins in Plant-Microbe Interactions. Plant Cell Physiol. 2019, 60, 1405–1419. [Google Scholar] [CrossRef] [PubMed]
  87. Pii, Y.; Mimmo, T.; Tomasi, N.; Terzano, R.; Cesco, S.; Crecchio, C. Microbial interactions in the rhizosphere: Beneficial influences of plant growth-promoting rhizobacteria on nutrient acquisition process. A review. Biol. Fertil. Soils 2015, 51, 403–415. [Google Scholar] [CrossRef]
  88. Pieterse, C.M.J.; Zamioudis, C.; Berendsen, R.L.; Weller, D.M.; Van Wees, S.C.M.; Bakker, P.A.H.M. Induced Systemic Resistance by Beneficial Microbes. Annu. Rev. Phytopathol. 2014, 52, 347–375. [Google Scholar] [CrossRef]
  89. Bulgarelli, D.; Schlaeppi, K.; Spaepen, S.; van Themaat, E.V.L.; Schulze-Lefert, P. Structure and Functions of the Bacterial Microbiota of Plants. Annu. Rev. Plant Biol. 2013, 64, 807–838. [Google Scholar] [CrossRef]
  90. Harrier, L.A.; Watson, C.A. The potential role of arbuscular mycorrhizal (AM) fungi in the bioprotection of plants against soil-borne pathogens in organic and/or other sustainable farming systems. Pest Manag. Sci. 2004, 60, 149–157. [Google Scholar] [CrossRef]
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Figure 1. The potential mechanisms by which arbuscular mycorrhizal fungi (AMF) and grass endophyte (Epichloë) infection affect host plant response to biotic and abiotic stress.
Figure 1. The potential mechanisms by which arbuscular mycorrhizal fungi (AMF) and grass endophyte (Epichloë) infection affect host plant response to biotic and abiotic stress.
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Shen, Y.; Duan, T. The Interaction between Arbuscular Mycorrhizal Fungi (AMF) and Grass Endophyte (Epichloë) on Host Plants: A Review. J. Fungi 2024, 10, 174. https://doi.org/10.3390/jof10030174

AMA Style

Shen Y, Duan T. The Interaction between Arbuscular Mycorrhizal Fungi (AMF) and Grass Endophyte (Epichloë) on Host Plants: A Review. Journal of Fungi. 2024; 10(3):174. https://doi.org/10.3390/jof10030174

Chicago/Turabian Style

Shen, Youlei, and Tingyu Duan. 2024. "The Interaction between Arbuscular Mycorrhizal Fungi (AMF) and Grass Endophyte (Epichloë) on Host Plants: A Review" Journal of Fungi 10, no. 3: 174. https://doi.org/10.3390/jof10030174

APA Style

Shen, Y., & Duan, T. (2024). The Interaction between Arbuscular Mycorrhizal Fungi (AMF) and Grass Endophyte (Epichloë) on Host Plants: A Review. Journal of Fungi, 10(3), 174. https://doi.org/10.3390/jof10030174

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