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Review

Antagonism to Plant Pathogens by Epichloë Fungal Endophytes—A Review

by
Stuart D. Card
1,*,
Daniel A. Bastías
1 and
John R. Caradus
2
1
AgResearch Limited, Grasslands Research Centre, Private Bag 11008, Palmerston North 4442, New Zealand
2
Grasslanz Technology Limited, Private Bag 11008, Palmerston North 4442, New Zealand
*
Author to whom correspondence should be addressed.
Plants 2021, 10(10), 1997; https://doi.org/10.3390/plants10101997
Submission received: 8 September 2021 / Revised: 18 September 2021 / Accepted: 23 September 2021 / Published: 24 September 2021
(This article belongs to the Special Issue Fungal Endophytes against Plant Pathogenic Fungi)
Versions Notes

Abstract

:
Epichloë is a genus of filamentous fungal endophytes that has co-evolved with cool-season grasses with which they form long-term, symbiotic associations. The most agriculturally important associations for pasture persistence for grazing livestock are those between asexual vertically transmitted Epichloë strains and the pasture species, perennial ryegrass, and tall fescue. The fungus confers additional traits to their host grasses including invertebrate pest deterrence and drought tolerance. Selected strains of these mutualistic endophytes have been developed into highly efficacious biocontrol products and are widely utilized within the Americas, Australia, and New Zealand for pasture persistence. Less publicized is the antagonism Epichloë endophytes display towards multiple species of saprophytic and pathogenic microbes. This opinion piece will review the current literature on antimicrobial properties exhibited by this genus of endophyte and discuss the reasons why this trait has historically remained a research curiosity rather than a trait of commercial significance.

1. Introduction

Most multicellular life on Earth lives in symbiosis with microorganisms [1]. Plants, for example, whether they are growing within natural or managed ecosystems, are constantly interacting with a myriad of living microorganisms, including archaea, bacteria, fungi, and protists, throughout their lifecycle [2]. This microbial community (the plant microbiota) coupled with the surrounding environment (the entire habitat = the microbiome) has distinct physio-chemical properties and is crucially important for the health and productivity of the host plant. The interactions between hosts and microbes, or symbiosis, are complex ranging from mutualism through commensalism to parasitism in a continuous manner [3,4] and are important ecological determinants of plant biodiversity [5], although some regard parasitism as an unbalanced status of the symbiosis [6]. Furthermore, mutualistic symbioses were likely responsible for early host plant habitat transitions in the late Precambrian era (ca. 600 Ma) with several microbial species implicated in the evolution of photosynthesizing organisms [7,8,9,10]. This concept forms the basis for the hologenome theory of evolution [11] and proposes that the holobiont, the plant host plus all of its symbionts, is a unit of selection [12]. Although the first mutualistic symbioses were likely to have been associations between simple monerans and protists that led to the Cambrian explosion [10], present day symbiosis are more diverse. Examples include lichens (associations between algae or cyanobacteria and several fungal species), those between rhizobia and legumes, mycorrhiza (those associations between plants and fungi), and associations between Epichloë fungal endophytes and cool-season grasses.

2. Epichloë Endophytes

Epichloë (family Clavicipitaceae) is a monophyletic genus of filamentous fungi that form perpetual symbioses with cool-season grasses (family Poaceae subfamily Pooideae) [13]. These endophytes are regarded as keystone species, being ecologically important constituents of many grassland ecosystems, which cover over 30% of the Earth’s land area and are, therefore, one of the largest biomes on the planet [14,15,16]. Epichloë species are naturally restricted to a host genus or closely related grass genera within a tribe as a result of co-evolution over many millennia [17,18,19]. However, this group of grass symbionts may have originally emerged from an animal pathogen via an interkingdom host jump [20,21]. As with most members of the Ascomycota, the genus Epichloë includes both anamorphic (asexual) and teleomorphic (sexual) species, with the former previously classified as Neotyphodium [22]. Over 30 species of Epichloë have been described [22] with most exhibiting an anamorphic lifecycle.
Obligatory sexual species of Epichloë are largely antagonistic to their host plant as the epiphytic stroma that is formed on the developing host inflorescence, essential for horizontal transmission, suppresses plant seed production, thereby impeding the hosts ability to reproduce [23]. In contrast, the asexual species are symptomless within their host plants being exclusively vertically transmitted via the host’s seed [24,25]. Many of the plant’s progeny inherit chromosomes and cytoplasm from their parents but also their mutualistic symbionts, constituting a form of hereditary endosymbiosis [26]. Epichloë have been documented to confer a multitude of beneficial attributes to their host grasses. These attributes differ across the various endophyte–host associations with the most prominent being protection from mammalian and invertebrate herbivory via the production of secondary metabolites, most notably alkaloids [27]. The major metabolites involved in this defensive mutualism include peramine, an insect feeding deterrent; the lolines, a group of saturated exo-1-amino pyrrolizidines that exhibit a broad spectrum of insecticidal activity; indole diterpenes and ergot alkaloids that contain classes of compound that exhibit toxicity towards both vertebrates and invertebrates [28]. Additional attributes include tolerance against abiotic stresses (i.e., when the plant is exposed to adverse environmental conditions) such as those caused by drought and/or nutrient deficiencies [29,30].
Epichloë endophytes were initially identified as the cause of a serious agriculture issue due to some endophyte-grass associations producing alkaloidal neurotoxins that are detrimental to many animal species, including livestock (i.e., farmed ruminants) [31]. The most potent of these compounds include the lolitrems (indole diterpenes) and ergot alkaloids that result in ryegrass staggers and heat stress/fescue-foot syndromes respectively [32,33,34]. Research on the Epichloë endophyte associations with Lolium perenne L. (perennial ryegrass) in New Zealand (NZ) and Lolium arundinaceum (Schreb.) S.J. Darbyshire (= Festuca arundinacea Schreb.; tall fescue) in the USA, identified asexual Epichloë strains that were less toxic to livestock whilst conferring advantageous traits to their host grasses. Since this initial research in the 1980s and 1990s, scientific programmes have been established that center on bioprospecting pipelines to identify, characterize and select agriculturally beneficial endophyte strains (those that confer advantageous traits to their host while producing little or no detrimental effects to grazing livestock) that could be incorporated into elite grass cultivars with increased pasture persistence and productivity [30,31].
AgResearch (a NZ government owned research institute that carries out scientific research for the benefit of NZ; https://www.agresearch.co.nz; accessed on 15 September 2021) developed bioprospecting pipelines that (1) identify Epichloë endophytes from global collections of germplasm, (2) characterize Epichloë isolates with respect to their genetic diversity, secondary metabolite profiles and bioactivity, (3) inoculate agriculturally useful strains with commercial potential into elite grass cultivars, and (4) evaluate populations of novel grass-endophyte associations through specifically designed agronomic and toxicological screens [35,36]. Endophyte strains that are devoid of lolitrems and ergot alkaloids while possessing insect-deterring compounds (e.g., peramine and/or lolines) generally have commercial potential. This opinion piece will review the current literature on the antimicrobial properties exhibited by Epichloë fungal endophytes and discuss the reasons why this trait has historically remained a research curiosity rather than a trait of commercial significance.

3. Interaction of Epichloë spp. with Plant Pathogens

Although a great deal of knowledge regarding the bioactivity of Epichloë-derived secondary metabolites on invertebrate pests has been gained, little research has been undertaken on the biological control of fungal phytopathogens by Epichloë-infected grasses [37,38]. To the best of our knowledge, no published research documents the biological control of bacterial phytopathogens by Epichloë, although certain endophyte strains can influence the host plant’s bacterial microbiota [39]. Furthermore, no correlation exists between the antifungal bioactivity expressed by these endophytes and their alkaloid profiles [40,41] and although several Epichloë-based grass products are marketed across the continents of Australia, North America and South America for their insect deterrent properties [30,31,42], none are marketed for their control of plant diseases. However, Epichloë endophytes can inhibit the growth and reproduction of other microorganisms, including economically important fungal phytopathogens [43]. A recent meta-analysis has shown that all species of phytopathogen significantly affected by the presence of Epichloë endophyte regardless of their lifestyle (biotrophic vs. necrotrophic), with both laboratory and greenhouse comparisons showing negative effects of Epichloë spp. on the growth and infection by phytopathogens [44]. However, many of the published reports describe bioactivity that has been assessed using crudely designed in vitro dual culture bioassays (Table 1), with fewer reports on this phenomenon in planta within a field situation (Table 2).
Biological control, in its simplest form, can be defined as applied ecology [88] and is an environmentally sound and effective means of reducing or mitigating viral, microbial, nematode, insect, mite, weed, and vertebrate pests in agriculture, aquatic, forest, natural resources, stored products, and urban environments. Many primary screens using artificial nutrient media are severely criticized as they do not closely resemble the final arena where biological control ultimately takes place. Subsequently, these primary screens, which can determine antagonism between an endophyte and a phytopathogen in vitro, are generally poor at predicting protection within live plant tissues [89,90]. For example, in vitro research conducted in Finland showed clear antifungal activity expressed by strains of Epichloë towards the speckled snow mold pathogen, Typhula ishikariensis, when grown on potato dextrose agar (PDA). However, in the subsequent field experiment, the endophyte-infected grasses were more susceptible to the pathogen than the endophyte-free control plants [63].
This lack of correlation between in vitro and in planta results may be due to multiple reasons: (1) some Epichloë-derived secondary metabolites are only produced in planta. For example, the endophyte-derived alkaloids are metabolites only produced by the grass-endophyte association with the exception of two loline alkaloids that can be produced in vitro from axenic endophyte cultures at a relatively low concentration from a defined minimal media [91], (2) concentrations of Epichloë-derived secondary metabolites depend on the host plant. These endophytes may not be able to secure the relevant nutrients or amount of nutrients in planta and the secondary metabolite biosynthetic pathways may be down regulated as with some biotrophic phytopathogens [92], and (3) the in vitro bioassays are largely restricted to identifying antibiosis as the sole mechanism of action exhibited by these fungi while other mechanisms exist. In vitro screens can, therefore, be misleading by either overestimating or underestimating the potential of endophyte strains to protect against phytopathogens.
Antibiosis is defined as antagonism mediated by specific or non-specific metabolites of microbial origin, by lytic agents, enzymes, volatile compounds or other toxic substances [88]. However, there are additional mechanisms of biological control proposed for Epichloë-plant associations [93], including induced resistance (reduced disease susceptibility of a plant in response to stimulation by a pathogen, insect herbivore, beneficial microbe, or chemical agent [94]) and competition for limiting factors (e.g., physical space, carbohydrates and amino acids) (see Table 2 for examples). The fourth main mechanism of biological control, direct parasitism, exhibited by several fungal antagonists such as Trichoderma spp. [95], has not been reported to date for Epichloë spp. The endophyte would have to engage in direct contact with the target phytopathogen, and this seems unlikely due to the restriction of these endophytes within the intracellular spaces of their grass hosts and the sometimes-suppressive nature of the regulation that they encounter during their growth and development [96,97].
As mentioned previously, no correlation exists between the antifungal bioactivity expressed by these endophytic fungi and their alkaloid profiles [40,41]. However, several non-alkaloid secondary metabolites have been implicated in the antagonism exhibited by Epichloë spp. towards phytopathogens (see antibiosis studies listed in Table 2). These compounds include sesquiterpenes [45,98], phenolic glycerides [99], hydroxyl unsaturated fatty acids [100], aromatic sterols [101], indole derivatives (indole-3-acetic acid (IAA) and indole-3-ethanol), diacetamides [45] and other volatile insect-attractant compounds, such as Chokol K and methyl esters [102]. Chokol K is an interesting compound, hypothesized to of originated as an antimicrobial agent the compound also has the ability to attract Botanophila flies, fungal pollinators of the external fruiting structures, the stroma, of sexually reproducing Epichloë species [103].
Research conducted on the bioactivity of Epichloë endophytes (Card, unpublished) aligns with previous studies in the literature that show that many Epichloë species exhibit antifungal activity towards a wide range of saprophytic and pathogenic fungal species, including those with diverse taxonomy (e.g., species from both the Ascomycota and Basidiomycota) and those with different lifestyles (e.g., biotrophs and necrotrophs) (Table 1 and Table 2). This could indicate that several antifungal compounds are produced simultaneously or that a small number of antifungal compounds have broad antifungal activity. Further work showed that no antifungal activity was attributed to guttation fluid collected from perennial ryegrass plants infected with selected Epichloë strains (Lambie and Christensen, unpublished) similar to that found with peramine against insects [104]. This may indicate that if antifungal compound/s are solely responsible for biological control within this system then they may have limited mobilization within the plant.
The Epichloë-mediated induction of the plant’s own defenses has been proposed as another mechanism of resistance against phytopathogens [43,44]. Plant defenses are regulated by hormonal signaling pathways, including salicylic acid (SA) and jasmonic acid (JA) [105]. The dominant model for conceptualizing plant defenses suggests that the SA and JA signaling pathways protect plants against biotrophic and necrotrophic pathogens, respectively [106]. Epichloë spp. can activate host plant SA- and JA-signaling pathways [107]. This Epichloë-based activation of plant defense hormonal signaling pathways may explain, at least in part, the increased levels of disease resistance exhibited by Epichloë-infected plants (see IR studies listed in Table 2). For example, enhanced plant resistance exhibited by endophyte-infected A. inebrians plants against the biotrophic pathogen B. graminis was related to the activation of SA signaling pathways, increment in SA levels, and the upregulation in the expression of SA-related genes coding for putative plant enzymes with antifungal activities (i.e., β-1,3-glucanase and callose synthase) [77]. Similarly, the enhanced plant resistance exhibited by A. sibiricum plants against the necrotrophic pathogen C. lunata by A. sibiricum was correlated to increased levels of JA and plant phenolics [79].
Further novel mechanisms have been proposed for specific grass-endophyte combinations, for example niche exclusion has been proposed for Epichloë associations with Bromus setifolius, Festuca ovina, F. rubra, and Poa ampla [108]. This mechanism results in the exclusion of phytopathogens by a superficial network of endophyte mycelium that develops on the leaf blade surface of grasses. The epiphytic mycelium was hypothesized to be defensive in function to physically exclude the entry of fungal pathogens into the leaves [109]. Pérez et al. [44] further proposed that two classes of mechanism exist with respect to the reduction of plant disease by Epichloë spp., (1) direct pathways mediated by antibiosis, competition and IR (described above) and (2) indirect pathways associated with endophyte-generated changes in either the abiotic or the biotic host environment. These authors describe an indirect pathway for the protection of L. multiflorum by its fungal endophyte E. occultans from the flower-infecting pathogen Claviceps purpurea, the causal agent of ergot [44]. The incidence and severity of C. purpurea infection was two-fold lower in endophyte-symbiotic plants than in non-symbiotic ones but when insects were prohibited from visiting the flowers this difference disappeared, indicating that endophyte-derived volatile compounds repel insect vectors of C. purpurea and indirectly defend their host grasses against plant disease [80].
Antagonism between Epichloë spp. and phytopathogens may have evolved many millions of years ago. A recent article describes an ancient cross-kingdom gene transfer (the transfer of genetic material between organisms) from Epichloë to tall wheatgrass (Thinopyrum ponticum). The article suggests that Fhb7, a major, semidominant resistance gene, was transferred to the wild cereal grass around 5 million years ago after the divergence of Thinopyrum from other grasses [110]. Fhb7 encodes a glutathione S-transferase that detoxifies deoxynivalenol (DON), a mycotoxin that renders grain poisonous to humans and other mammals. It is speculated that Epichloë may have evolved Fhb7 to compete with Fusarium spp. for grass colonization [111]. Furthermore, transcriptomic studies have identified an abundantly expressed fungal gene coding for a small, secreted protein, similar to antifungal proteins found within species of Penicillium and Aspergillus, in Epichloë festucae-infected red fescue plants [112]. The antifungal protein gene is not found within the genomes of many other Epichloë spp. and is hypothesized to be a component of the unique disease resistance observed with endophyte-infected red fescue plants to dollar spot disease caused by the phytopathogen Clarireedia jacksonii [113]. It is suggested that once the endophyte lifestyle evolved in Epichloë, and the wider Clavicipitaceae endophytes, the alkaloid and other fungal–mediated defensive features adapted from previous functions to serve as plant host defense functions [114].
Recent theoretical modelling studies suggested that in order to predict biocontrol outcomes there is a need to understand not only the main biocontrol mechanisms involved but also the extent of environmental variability, the level of biocontrol activity, and survival of individual biological control agents in relation to external conditions [115]. Epichloë fungi, and other mutualistic endophytes, have a distinctive advantage over other biocontrol microorganisms that are inoculated into the phyllosphere or rhizosphere through drenches or sprays. By inhabiting the intracellular spaces of their plant hosts for their entire lifecycle they are buffeted from many cyclic and non-cyclic variables, including potentially damaging ultraviolet rays, extremes of temperature, humidity, dew, rain and wind as experienced, for example, on the leaf surface [88]. Endophytic microorganisms are also protected from faster proliferating, more competitive microorganisms as experienced in many phyllosphere and rhizosphere environments. Endophyte survival is firmly tied with that of the plant host and are therefore totally reliant on the plant for substrates (e.g., water, sugars, and oxygen) and a suitable ecological niche free from competing microorganisms, along with the absence of inhibitory or toxic substances. While nutrients may become limiting in the phyllosphere environment, endophytes are supplied with a bountiful array of organic and inorganic nutrients including sugars, sugar alcohols, nitrates, nitrites, amino acids, organic acids, calcium, chloride, phosphorus, potassium, sulfur and soluble proteins [as reviewed by 116] supplied to the apoplasm from the neighboring phloem. Although the concentration and availability of such compounds within the apoplasm may fluctuate, it is largely a copiotrophic environment [116]. Substrates are not only in plentiful supply to support endophyte growth (biomass) but also may support the production of many secondary metabolites, including many anti-mammalian and insect deterrent alkaloidal compounds [28] as well as antimicrobial compounds active against phytopathogens.
The inhibition of phytopathogens by Epichloë has, however, largely remained a research curiosity rather than an attribute exploited for commercial disease biocontrol purposes as very few in planta experiments document the control of economically important phytopathogens in the field. These may be due to several reasons:
(1)
Many phytopathogens, particularly foliar fungal pathogens, are notoriously difficult to control (even by conventional synthetic agrichemicals) as they can produce vast numbers of wind-disseminated spores that are spread over large distances over significant periods of time. These phytopathogens can also exhibit a polycyclic nature that can be completed in just a few days, continuously barraging the plant with fresh inoculum.
(2)
Many plant diseases occur due to underlying abiotic disorders (e.g., nutrient imbalance, and/or water stress) that have weakened or stressed the plant and made it susceptible to invasion by a phytopathogen. Additionally, disease in the field is generally brought about by a complex of interacting microorganisms including primary and secondary pathogens making identification of the causal organism difficult.
(3)
Bioprospecting pipelines have to date identified Epichloë strains with deterrent traits against economically important invertebrate pests and therefore endophyte strains with high levels of bioactivity towards phytopathogens could have been missed, overlooked, or not prioritised.
(4)
Many in vitro primary screens overestimate the bioactivity of selected endophyte strains and do not screen enough strains to identify those with high potential for commercialisation. Great strain variation exists with respect to antifungal activity [53] and even morphotypes of the same species from the same host grass species can vary in their antifungal activity [37]. Furthermore, host genotype × endophyte effects can impact the degree of antifungal activity expressed.
(5)
A lack of understanding concerning the mechanisms of action attributed to selected Epichloë strains. These mechanisms need to be understood to develop suitable novel grass-endophyte associations.
(6)
Many end users completely ignore the concept of biological control in favour of agrichemicals while others view it as essentially a compete synthetic chemistry replacement. However, biological control products have been generally less reliable than agrichemicals which has hampered their development, release, and commercial uptake [117]. For example, Epichloë strains with antifungal activity will generally only reduce the frequency or size of diseased lesions and, therefore, disease is still present [53].

4. Interaction of Epichloë Endophytes with Other Taxa

As well as fungal phytopathogens, Epichloë, or their metabolites, can influence the interactions between endophyte-infected plants and other organisms. As discussed, endophyte-derived alkaloids can influence invertebrates and species such as herbivorous mammals and this in turn can affect species diversity and fundamental ecological processes like decomposition, and food web structures [118,119,120,121,122]. In natural ecosystems, Epichloë can reduce plant diversity, enhance the dominance of certain grass-endophyte associations [5] and also generate legacy effects which persist after the death of the host [123]. Epichloë endophytes may also impact the microbiome (the microbiota and its theatre of activity) of the vegetative host plant effecting microbial community structure in above and below ground habitats [121]. Studies aimed at investigating the rhizosphere communities of tall fescue plants show that Epichloë-infected plants showed a higher species richness over endophyte-free rhizospheres and a greater percentage of Firmicutes [124] while the presence of Epichloë gansuensis within its host grass Achnatherum inebrians significantly decreased root-associated fungal diversity [125]. These findings within the rhizosphere are paralleled within the phyllosphere where some endophyte-infected fescue species select particular epiphytic bacterial microbiota [39] with loline alkaloids implicated as a significant carbon source for certain bacterial genera including Burkholderia, Serratia, Pseudomonas and Stenotrophomonas [124]. In the rhizosphere, strains of these bacterial taxa have subsequently been shown to outcompete and suppress the growth of non-loline catabolizing strains [124]. Epichloë endophytes can also impact plant reproduction with endophyte-infected seed harbouring higher populations of plant-growth promoting bacteria compared to endophyte-free varieties, with these bacteria possibly playing an important role in the fitness of the subsequent seedlings [126]. Further work is looking at how Epichloë endophytes may shape entire ecological communities [15,127].
A substantial amount of research has investigated the interaction between Epichloë species and well-known beneficial microorganisms, such as arbuscular mycorrhizal (AM) fungi [128]. AM fungi aid the host by supplying mineral nutrients (mostly phosphorus) improving the nutritional status of colonised plants while also increasing the host’s tolerance to certain abiotic and biotic stresses [4,129]. In planta studies investigating the interaction between Epichloë endophytes and AM fungi show that the amount by which symbiotic plant roots are colonised by AM fungi depends on the type of grass-Epichloë association [130]. For example, agronomic, novel grass-Epichloë associations often have lower amounts of mycorrhizal mycelia in roots of symbiotic plants (i.e., artificial symbioses: L. perenne-E. festucae var. lolii, Lolium multiflorum-Epichloë occultans, and F. arundinacea-E. coenophiala) while wild grasses infected with their co-evolved Epichloë endophytes usually display greater abundances of AM fungi in roots of symbiotic plants (i.e., Bromus spp. and Poa spp.) [131,132,133,134,135,136,137,138,139,140]. Further complexities also exist with regard to species interactions [141,142]. Epichloë-derived bioactive compounds, competition for nutrients, and/or changes in the levels of plant resistance to microorganisms have been proposed as mechanisms to explain the interaction between Epichloë and AM fungi [137].
Recent research from NZ has also determined that Epichloë strains can associate closely with specific bacterial species [143] and may work in synergy to antagonise microorganisms that threaten the survival and reproduction of the host plant. This has been shown in other tripartite interactions within multiple fungal species [144] with bacterial endosymbionts responsible for mycotoxin and phytohormone production including IAA [145,146]. IAA is the major plant auxin and is also synthesized by certain microorganisms, including phytopathogens, saprophytes and symbionts [147]. IAA stimulates the production of plant biomass, enhances growth rate of roots, and is implicated in the promotion of disease resistance [147,148]. Tripartite associations involving Epichloë endophytes are not restricted to bacteria with several articles reporting that Epichloë spp. can also be infected with mycoviruses [149,150,151]. Although these viruses appear to have no effect on the phenotype of their fungal hosts, the fungus, or plant infected by the endophytic fungus and the virus, may obtain selective advantages yet to be discovered.

5. Future Perspectives

Climate change, the most important challenge currently facing mankind [152] is predicted to have serious implications for many agricultural systems. The interaction between disease and crops is as old as agriculture itself [153] but with increasing temperatures and changing precipitation patterns, it is expected that plant disease outbreaks may intensify in some production areas due to invasions of new phytopathogens and/or due to increases in the severity of existing phytopathogens [154,155,156]. Increasing atmospheric CO2 levels will impact the degree of resistance exhibited by many plant species to pathogen attack while also altering the availability of photosynthates and defensive compounds produced by plant-associated microorganisms, including Epichloë [66,157,158]. For example, when CO2 was artificially elevated, the beneficial effect of Epichloë on its tall fescue host was lost with respect to plant growth and pathogen resistance towards C. lunata [66]. Other gases involved in climate change, such as tropospheric ozone, have also been shown to have detrimental effects on plant host fitness and the concentration of Epichloë -derived defense compounds [159].
Further challenges include improving and/or changing current agricultural practices that are not sustainable as they can expend valuable resources while degrading the environment [160]. Many agrichemicals have negative effects on the environment due to overuse and inefficient application [161] while the control of plant diseases using synthetic pesticides raises serious concerns about food safety, environmental quality and pathogen resistance [162]. Coupled with other pastoral management practices (e.g., tillage), this has also led to a decrease in soil biodiversity [163] in many regions worldwide. Integrating knowledge from both agricultural and natural ecosystems, from single plants and multispecies plant communities, and from below-ground and above-ground multitrophic interactions holds great promise to further improve the sustainability of crop production, including the need for alternative disease management practices [164].
While Epichloë endophytes are not naturally found in modern cereal grasses it has been demonstrated that Epichloë strains from wild cereal grass relatives [165] can be inoculated into barley (Hordeum vulgare), rye (Secale cereale) and wheat (Triticum aestivum) to create artificial plant-endophyte associations [166,167,168]. Field trials with Epichloë-infected rye have shown reductions in the prevalence of leaf rust (Puccinia recondita) and leaf streak (Cercosporidium graminis) [65]. The potential for other fungal endophyte taxa to be used as biological control agents against phytopathogens in rice, wheat and maize has been proposed as a worthy research aim [169].

6. Concluding Remarks

Microorganisms have been administered as biological control agents for many decades to manage disease and pest pressures on crop plants. However, they still only make up a small percentage of all pest control products. As well as their overall bioactivity and efficacy in the field, many other factors (such as their stability, reliability, storage and application) must be taken into consideration for the development of commercially successful biological control agents [170]. Endophytes can overcome many of the difficulties faced by traditional biological control agents as they are encapsulated within the host plant and protected from environmental conditions that disrupt their survival and biocontrol efficacy. Additionally, for those biocontrol agents that are seed transmitted, such as Epichloë endophytes, there is an extra advantage for commercialisation as there is no need to develop complicated formulations and delivery techniques [171]. Biological control of phytopathogens is often achieved by the artificial introduction of antagonistic microorganisms into a selected environment. These antagonists may exhibit several mechanisms of action that work in synergy to suppress any one phytopathogen at any one time and although Epichloë-derived antibiosis may be overrepresented in many in vitro experiments this mechanism may still play a pivotal role in the protection of grass hosts from phytopathogens. Although Epichloë endophyte colonization is generally restricted to the host’s aboveground tissues, their bioactivity (at least towards invertebrate herbivores, via antibiosis) extends further, as many endophyte-derived alkaloids are mobilized within the plant’s vascular system and translocated to plant organs, such as the roots, where fungal colonization is absent [119,172]. Even volatile secondary metabolites derived from Epichloë endophytes have been reported in the roots of endophyte-infected plants [173,174].
Therefore, primary in vitro bioassays, aimed at assessing endophytes for their antagonism towards phytopathogens, must be developed to provide more reliable predictions of field performance [175]. The results from these improved bioassays, coupled with a greater understanding of the mechanisms of action attributed to these Epichloë endophytes, will likely lead to the development of ecologically sound and commercially viable Epichloë-grass associations with pest and disease control abilities.

Author Contributions

Conceptualization, S.D.C. and J.R.C., writing—original draft preparation, S.D.C.; writing—review and editing, S.D.C., D.A.B. and J.R.C.; All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

All data are included in the present study.

Acknowledgments

We would like to thank Christina Moon for critical revision of the manuscript.

Conflicts of Interest

J.R.C. is employed by Grasslanz Technology Limited, a company that is a part-owner of the intellectual property associated with Epichloë strains marketed under the brands AR1TM, AR37TM, Endo5TM, MaxQTM, MaxQIITM, MaxPTM, MaxRTM, AvanexTM, Happe and Protek.

References

  1. Rodriguez, R.; Redman, R. More than 400 million years of evolution and some plants still can’t make it on their own: Plant stress tolerance via fungal symbiosis. J. Exp. Bot. 2008, 59, 1109–1114. [Google Scholar] [CrossRef] [PubMed]
  2. Zipfel, C.; Oldroyd, G.E.D. Plant signalling in symbiosis and immunity. Nature 2017, 543, 328–336. [Google Scholar] [CrossRef] [PubMed]
  3. Redman, R.S.; Dunigan, D.D.; Rodriguez, R.J. Fungal symbiosis from mutualism to parasitism: Who controls the outcome, host or invader? New Phytol. 2001, 151, 705–716. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  4. Partida-Martinez, L.P.P.; Heil, M. The microbe-free plant: Fact or artifact? Front. Plant Sci. 2011, 2, 100. [Google Scholar] [CrossRef] [Green Version]
  5. Clay, K.; Holah, J. Fungal endophyte symbiosis and plant diversity in successional fields. Science 1999, 285, 1742–1744. [Google Scholar] [CrossRef]
  6. Kogel, K.-H.; Franken, P.; Hückelhoven, R. Endophyte or parasite—What decides? Curr. Opin. Plant Biol. 2006, 9, 358–363. [Google Scholar] [CrossRef]
  7. Heckman, D.S.; Geiser, D.M.; Eidell, B.R.; Stauffer, R.L.; Kardos, N.L.; Hedges, S.B. Molecular evidence for the early colonization of land by fungi and plants. Science 2001, 293, 1129–1133. [Google Scholar] [CrossRef] [Green Version]
  8. Margulis, L. Symbiosis and evolution. Sci. Am. 1971, 225, 48–61. [Google Scholar] [CrossRef]
  9. Remy, W.; Taylor, T.N.; Hass, H.; Kerp, H. Four hundred-million-year-old vesicular arbuscular mycorrhizae. Proc. Natl. Acad. Sci. USA 1994, 91, 11841–11843. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  10. Pirozynski, K.A.; Malloch, D.W. The origin of land plants: A matter of mycotrophism. Biosystems 1975, 6, 153–164. [Google Scholar] [CrossRef]
  11. Rosenberg, E.; Sharon, G.; Zilber-Rosenberg, I. The hologenome theory of evolution contains Lamarckian aspects within a Darwinian framework. Environ. Microbiol. 2009, 11, 2959–2962. [Google Scholar] [CrossRef]
  12. Rosenberg, E.; Sharon, G.; Atad, I.; Zilber-Rosenberg, I. The evolution of animals and plants via symbiosis with microorganisms. Environ. Microbiol. Rep. 2010, 2, 500–506. [Google Scholar] [CrossRef] [PubMed]
  13. Johnson, L.J.; Bastias, D.A.; Caradus, J.R.; Chettria, P.; Forester, N.T.; Mace, W.J.; Miller, T.A.; Moon, C.D.; Voisey, C.R.; Zhang, W.; et al. The dynamic mechanisms underpinning symbiotic Epichloë—Grass interactions: Implications for sustainable and resilient agriculture. In Microbiome Stimulants for Crops: Mechanisms and Applications; White, J., Kumar, A., Droby, S., Eds.; Woodhead Publishing: Sawston, UK, 2021. [Google Scholar]
  14. Suttie, J.M.; Reynolds, S.G.; Batello, C. Grasslands of the World; Food & Agriculture Organization: Rome, Italy, 2005; Volume 34. [Google Scholar]
  15. Nissinen, R.; Helander, M.; Kumar, M.; Saikkonen, K. Heritable Epichloë symbiosis shapes fungal but not bacterial communities of plant leaves. Sci. Rep. 2019, 9, 5253. [Google Scholar] [CrossRef]
  16. Gibson, D.J. Grasses and Grassland Ecology; Oxford University Press: Oxford, UK, 2009. [Google Scholar]
  17. Schardl, C.L. The epichloae, symbionts of the grass subfamily poöideae. Ann. Mo. Bot. Gard. 2010, 97, 646–665. [Google Scholar] [CrossRef]
  18. Schardl, C.L.; Leuchtmann, A.; Chung, K.-R.; Penny, D.; Siegel, M.R. Coevolution by common descent of fungal symbionts (Epichloë spp.) and grass hosts. Mol. Biol. Evol. 1997, 14, 133–143. [Google Scholar] [CrossRef] [Green Version]
  19. Schardl, C.L.; Phillips, T.D. Protective grass endophytes: Where are they from and where are they going? Plant Dis. 1997, 81, 430–438. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  20. Spatafora, J.; Sung, G.; Sung, J.; Hywel-Jones, N.; White, J.F., Jr. Phylogenetic evidence for an animal pathogen origin of ergot and the grass endophytes. Mol. Ecol. 2007, 16, 1701–1711. [Google Scholar] [CrossRef]
  21. Sung, G.-H.; Poinar, G.O.; Spatafora, J.W. The oldest fossil evidence of animal parasitism by fungi supports a Cretaceous diversification of fungal–arthropod symbioses. Mol. Phylogenet. Evol. 2008, 49, 495–502. [Google Scholar] [CrossRef]
  22. Leuchtmann, A.; Bacon, C.W.; Schardl, C.L.; White, J.F.; Tadych, M. Nomenclatural realignment of Neotyphodium species with genus. Epic. Mycol. 2014, 106, 202–215. [Google Scholar] [CrossRef]
  23. Chung, K.-R.; Schardl, C. Sexual cycle and horizontal transmission of the grass symbiont Epichloë typhina. Mycol. Res. 1997, 101, 295–301. [Google Scholar] [CrossRef]
  24. 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] [PubMed]
  25. Liu, J.; Nagabhyru, P.; Schardl, C.L. Epichloë festucae endophytic growth in florets, seeds, and seedlings of perennial ryegrass (Lolium perenne). Mycologia 2017, 109, 691–700. [Google Scholar] [CrossRef] [PubMed]
  26. Wernegreen, J.J. Endosymbiosis. Curr. Biol. 2012, 22, R555–R561. [Google Scholar] [CrossRef] [Green Version]
  27. Clay, K. Fungal endophytes of grasses: A defensive mutualism between plants and fungi. Ecology 1988, 69, 10–16. [Google Scholar] [CrossRef]
  28. 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]
  29. Caradus, J.R.; Johnson, L.J. Improved adaptation of temperate grasses through mutualism with fungal endophytes. In Endophyte Biotechnology: Potential for Agriculture and Pharmacology; Schouten, A., Ed.; CABI: Wageningen, The Netherlands, 2019; pp. 85–108. [Google Scholar]
  30. Johnson, L.J.; Caradus, J.R. The science required to deliver Epichloë endophytes to commerce. Endophytes Grow. World 2019, 343–370. [Google Scholar] [CrossRef]
  31. Johnson, L.; de Bonth, A.; Briggs, L.; Caradus, J.; Finch, S.; Fleetwood, D.; Fletcher, L.; Hume, D.; Johnson, R.; Popay, A.J.; et al. The exploitation of epichloae endophytes for agricultural benefit. Fungal Divers. 2013, 60, 171–188. [Google Scholar] [CrossRef]
  32. Caradus, J.R.; Card, S.D.; Finch, S.C.; Hume, D.E.; Johnson, L.J.; Mace, W.J.; Popay, A.J. Ergot alkaloids in New Zealand pastures and their impact. N. Z. J. Agric. Res. 2020, 63, 1–41. [Google Scholar] [CrossRef]
  33. Gallagher, R.T.; White, E.P.; Mortimer, P.H. Ryegrass staggers: Isolation of potent neurotoxins lolitrem A and lolitrem B from staggers-producing pastures. N. Z. Vet. J. 1981, 29, 189–190. [Google Scholar] [CrossRef]
  34. Bacon, C.W.; Porter, J.K.; Robbins, J.D.; Luttrell, E.S. Epichloë typhina from toxic tall fescue grasses. Appl. Environ. Microbiol. 1977, 34, 576–581. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  35. Card, S.; Johnson, L.; de Bonth, A.; Tapper, B.; Mace, W.; Faville, M.; Pennell, C.; Caradus, J.; Hume, D. Epichloë endophytes from cool season grasses–reaping the rewards from a well-tuned bio-prospecting pipeline. In Proceedings of the 10th International Mycological Congress, Bangkok, Thailand, 3–8 August 2014. [Google Scholar]
  36. De Bonth, A.; Card, S.; Briggs, L.; Faville, M.; Finch, S.; Hong, W.; Johnson, L.; Liu, L.; Mace, W.; Pennell, C. Fungal foray: The pursuit of beneficial endophyte strains for Australasian pastures. In Proceedings of the 9th International Symposium on Fungal Endophytes of Grasses, Melbourne, VIC, Australia, 28 September–1 October 2015. [Google Scholar]
  37. Ren, A.-Z.; Wang, Y.-H.; Gao, Y.-B. Difference in antifungal activity of morphotypes of clavicipitaceous endophytes within and between species. Acta Ecol. Sin. 2009, 29, 227–231. [Google Scholar] [CrossRef]
  38. Tian, P.; Nan, Z.; Li, C.; Spangenberg, G. Effect of the endophyte Neotyphodium lolii on susceptibility and host physiological response of perennial ryegrass to fungal pathogens. Eur. J. Plant Pathol. 2008, 122, 593–602. [Google Scholar] [CrossRef]
  39. Roberts, E.; Lindow, S. Loline alkaloid production by fungal endophytes of Fescue species select for particular epiphytic bacterial microflora. ISME J. 2014, 8, 359–368. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  40. Siegel, M.R.; Latch, G.C.M. Expression of antifungal activity in agar culture by isolates of grass endophytes. Mycologia 1991, 83, 529–537. [Google Scholar] [CrossRef]
  41. Christensen, M.J. Antifungal activity in grasses infected with Acremonium and Epichloë endophytes. Australas. Plant Pathol. 1996, 25, 186–191. [Google Scholar] [CrossRef]
  42. Caradus, J.R.; Johnson, L.J. Epichloë fungal endophytes—From a biological curiosity in wild grasses to an essential component of resilient high performing ryegrass and fescue pastures. J. Fungi 2020, 6, 322. [Google Scholar] [CrossRef]
  43. Xia, C.; Li, N.; Zhang, Y.; Li, C.; Zhang, X.; Nan, Z. Role of Epichloë endophytes in defense responses of cool-season grasses to pathogens: A review. Plant Dis. 2018, 102, 2061–2073. [Google Scholar] [CrossRef] [Green Version]
  44. Pérez, L.I.; Gundel, P.E.; Zabalgogeazcoa, I.; Omacini, M. An ecological framework for understanding the roles of Epichloë endophytes on plant defenses against fungal diseases. Fungal Biol. Rev. 2020, 34, 115–125. [Google Scholar] [CrossRef]
  45. Yue, Q.; Miller, C.J.; White, J.F., Jr.; Richardson, M.D. Isolation and characterization of fungal inhibitors from Epichloë festucae. J. Agric. Food Chem. 2000, 48, 4687–4692. [Google Scholar] [CrossRef]
  46. Yawen, J.; Rui, Z.; Xingxu, Z. Antagonistic effect of Epichloë bromicola of Hordeum brevisubulatum on a pathogenic fungus. In Proceedings of the 10th International Symposium on Fungal Endophytes of Grasses, Salamanca, Spain, 18–21 June 2018. [Google Scholar]
  47. White, J.F., Jr.; Cole, G.T. Endophyte-host associations in forage grasses. III. In vitro inhibition of fungi by Acremonium Coenophialum. Mycologia 1985, 77, 487–489. [Google Scholar] [CrossRef]
  48. White, J.F., Jr.; Cole, G.T. Endophyte-host associations in forage grasses. IV. The endophyte of Festuca versuta. Mycologia 1986, 78, 102–107. [Google Scholar] [CrossRef]
  49. Pańka, D.; West, C.; Guerber, C.; Richardson, M. Susceptibility of tall fescue to Rhizoctonia zeae infection as affected by endophyte symbiosis. Ann. Appl. Biol. 2013, 163, 257–268. [Google Scholar] [CrossRef]
  50. Li, C.; Gao, J.; Nan, Z. Interactions of Neotyphodium gansuense, Achnatherum inebrians and plant pathogenic fungi. Mycol. Res. 2007, 111, 1220–1227. [Google Scholar] [CrossRef]
  51. Gwinn, K.D.; Gavin, A.M. Relationship between endophyte infestation level of tall fescue seed lots and Rhizoctonia zeae seedling disease. Plant Dis. 1992, 76, 911–914. [Google Scholar] [CrossRef]
  52. Fernando, K.; Reddy, P.; Hettiarachchige, I.K.; Spangenberg, G.C.; Rochfort, S.J.; Guthridge, K.M. Novel antifungal activity of Lolium-associated Epichloë endophytes. Microorganisms 2020, 8, 955. [Google Scholar] [CrossRef]
  53. Niones, J.T.; Takemoto, D. An isolate of Epichloë festucae, an endophytic fungus of temperate grasses, has growth inhibitory activity against selected grass pathogens. J. Gen. Plant Pathol. 2014, 80, 337–347. [Google Scholar] [CrossRef]
  54. Purev, E.; Kondo, T.; Takemoto, D.; Niones, J.T.; Ojika, M. Identification of ε-Poly-L-lysine as an antimicrobial product from an Epichloë endophyte and isolation of fungal ε-PL synthetase gene. Molecules 2020, 25, 1032. [Google Scholar] [CrossRef] [Green Version]
  55. Niones, J.T.; Takemoto, D. VibA, a homologue of a transcription factor for fungal heterokaryon incompatibility, is involved in antifungal compound production in the plant-symbiotic fungus Epichloe festucae. Eukaryot. Cell 2015, 14, 13–24. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  56. Clarke, B.B.; White, J.F., Jr.; Hurley, R.H.; Torres, M.S.; Sun, S.; Huff, D.R. Endophyte-mediated suppression of dollar spot disease in fine fescues. Plant Dis. 2006, 90, 994–998. [Google Scholar] [CrossRef] [Green Version]
  57. Pańka, D.; Jeske, M.; Troczyński, M. Occurrence of Neotyphodium and Epichloë fungi in meadow fescue and red fescue in Poland and screening of endophyte isolates as potential biological control agents. Acta Sci. Pol. Hortorum Cultus 2013, 12, 67–83. [Google Scholar]
  58. Christensen, M.; Latch, G.; Tapper, B. Variation within isolates of Acremonium endophytes from perennial rye-grasses. Mycol. Res. 1991, 95, 918–923. [Google Scholar] [CrossRef]
  59. Holzmann-Wirth, A.; Dapprich, P.; Eierdanz, S.; Heerz, D.; Paul, V. Anti-fungal substances extracted from Neotyphodium endophytes. In Proceedings of the 3rd International Conference on Harmful and Beneficial Microorganisms in Grassland, Pasture and Turf, Soest, Germany, 26 September 2000. [Google Scholar]
  60. Pérez, L.I.; Gundel, P.E.; Omacini, M. Can the defensive mutualism between grasses and fungal endophytes protect non-symbiotic neighbours from soil pathogens? Plant Soil 2016, 405, 289–298. [Google Scholar] [CrossRef]
  61. Zhou, L.; Zhang, X.; Li, C.; Christensen, M.J.; Nan, Z. Antifungal activity and phytochemical investigation of the asexual endophyte of Epichloë sp. from Festuca sinensis. Sci. China Life Sci. 2015, 58, 821. [Google Scholar] [CrossRef] [Green Version]
  62. Lian-Yu, Z.; Song, Z.; Hong-Mei, D.; Feng, Q. Antimicrobial activity and composition of volatile substance of Epichloë sp. endophyte isolated from Festuca sinensis. Nat. Prod. Res. Dev. 2019, 31, 1543. [Google Scholar]
  63. Wäli, P.R.; Helander, M.; Nissinen, O.; Saikkonen, K. Susceptibility of endophyte-infected grasses to winter pathogens (snow molds). Botany 2006, 84, 1043–1051. [Google Scholar] [CrossRef]
  64. Wang, X.; Qin, J.; Chen, W.; Zhou, Y.; Ren, A.; Gao, Y. Pathogen resistant advantage of endophyte-infected over endophyte-free Leymus chinensis is strengthened by pre-drought treatment. Eur. J. Plant Pathol. 2016, 144, 477–486. [Google Scholar] [CrossRef]
  65. Hume, D.E.; Drummond, J.B.; Rolston, M.P.; Simpson, W.R.; Johnson, R.D. Epichloë endophyte improves agronomic performance and grain yield of rye (Secale cereale). In Proceedings of the 10th International Symposium on Fungal Endophytes of Grasses, Salamanca, Spain, 18–21 June 2018. [Google Scholar]
  66. Chen, W.; Liu, H.; Gao, Y.; Card, S.D.; Ren, A. The advantages of endophyte-infected over uninfected tall fescue in the growth and pathogen resistance are counteracted by elevated CO2. Sci. Rep. 2017, 7, 1–12. [Google Scholar] [CrossRef]
  67. Bonos, S.A.; Wilson, M.M.; Meyer, W.A.; Funk, C.R. Suppression of red thread in fine fescues through endophyte-mediated resistance. Appl. Turfgrass Sci. 2005, 2, 1–7. [Google Scholar] [CrossRef]
  68. 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]
  69. Li, F.; Duan, T.; Li, Y. Effects of the fungal Endophyte Epichloë festucae var. lolii on growth and physiological responses of perennial ryegrass cv. Fairway to combined drought and pathogen stresses. Microorganisms 2020, 8, 1917. [Google Scholar] [CrossRef]
  70. Pańka, D.; Piesik, D.; Jeske, M.; Baturo-Cieśniewska, A. Production of phenolics and the emission of volatile organic compounds by perennial ryegrass (Lolium perenne L.)/Neotyphodium lolii association as a response to infection by Fusarium Poae. J. Plant Physiol. 2013, 170, 1010–1019. [Google Scholar] [CrossRef]
  71. Lowe, K.F.; Bowdler, T.M.; Hume, D.E.; Casey, N.D.; Tapper, B.A. The effect of endophyte on the performance of irrigated perennial ryegrasses in subtropical Australia. Aust. J. Agric. Res. 2008, 59, 567–577. [Google Scholar] [CrossRef]
  72. 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]
  73. Wheatley, W.M.; Nicol, H.I.; Hunt, E.R.; Nikandrow, A.; Cother, N. An association between perennial ryegrass endophyte, a leafspot caused by (Pyrenophora seminiperda) and preferential grazing by sheep. In Proceedings of the 3rd International Conference on Harmful and Beneficial Microorganisms in Grassland, Pastures and Turf, Soest, Germany, 26 September 2000. [Google Scholar]
  74. Liu, L.; Guo, C.; Lv, H.; Gu, L.; Li, C. Effects of the Epichloë gansuensis endophyte on the disease resistance of drunken horse grass to powdery mildew. Acta Prataculturae Sin. 2015, 24, 65–71. [Google Scholar]
  75. 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]
  76. Xia, C.; Li, N.; Zhang, X.; Feng, Y.; Christensen, M.J.; Nan, Z. An Epichloë endophyte improves photosynthetic ability and dry matter production of its host Achnatherum inebrians infected by Blumeria graminis under various soil water conditions. Fungal Ecol. 2016, 22, 26–34. [Google Scholar] [CrossRef]
  77. Kou, M.-Z.; Bastías, D.A.; Christensen, M.J.; Zhong, R.; Nan, Z.-B.; Zhang, X.-X. The plant salicylic acid signalling pathway regulates the infection of a biotrophic pathogen in grasses associated with an Epichloë endophyte. J. Fungi 2021, 7, 633. [Google Scholar] [CrossRef]
  78. Zhang, H.; Li, X.; White, J.F.; Wei, X.; He, Y.; Li, C. Epichloë endophyte improves ergot disease resistance of host (Achnatherum inebrians) by regulating leaf senescence and photosynthetic capacity. J. Plant Growth Regul. 2021, 1–10. [Google Scholar] [CrossRef]
  79. Shi, X.; Qin, T.; Liu, H.; Wu, M.; Li, J.; Shi, Y.; Gao, Y.; Ren, A. Endophytic fungi activated similar defense strategies of Achnatherum sibiricum host to different trophic types of pathogens. Front. Microbiol. 2020, 11, 1607. [Google Scholar] [CrossRef] [PubMed]
  80. Perez, L.I.; Gundel, P.E.; Marrero, H.J.; Arzac, A.G.; Omacini, M. Symbiosis with systemic fungal endophytes promotes host escape from vector-borne disease. Oecologia 2017, 184, 237–245. [Google Scholar] [CrossRef]
  81. Wang, Y.; Luo, Y.; Tian, P.; Peng, H.; Feng, J. Preliminary evaluation of the disease resistance of Festuca sinensis infected by Epichloë sinensis. J. Phytopathol. 2021, 169, 623–629. [Google Scholar] [CrossRef]
  82. Iannone, L.J.; Vignale, M.V.; Pinget, A.D.; Re, A.; Cargo, P.D.M.; Novas, M.V. Seed-transmitted Epichloë sp. endophyte alleviates the negative effects of head smut of grasses (Ustilago bullata) on Bromus Auleticus. Fungal Ecol. 2017, 29, 45–51. [Google Scholar] [CrossRef]
  83. Kauppinen, M.; Helander, M.; Anttila, N.; Saloniemi, I.; Saikkonen, K. Epichloë endophyte effects on leaf blotch pathogen (Rhynchosporium sp.) of tall fescue (Schedonorus phoenix) vary among grass origin and environmental conditions. Plant Ecol. Divers. 2018, 11, 625–635. [Google Scholar] [CrossRef]
  84. Wiewióra, B.; Żurek, G.; Żurek, M. Endophyte-mediated disease resistance in wild populations of perennial ryegrass (Lolium perenne). Fungal Ecol. 2015, 15, 1–8. [Google Scholar] [CrossRef]
  85. Greulich, F.; Horio, E.; Shimanuki, T.; Yoshihara, T. Field results confirm natural plant protection by the endophytic fungus Epichloë typhina against the pathogenic fungus Cladosporium phlei on timothy leaves. Jpn. J. Phytopathol. 1999, 65, 454–459. [Google Scholar] [CrossRef] [Green Version]
  86. Shimanuki, T. Studies on the mechanisms of the infection of timothy with purple spot disease caused by Cladosporium phlei (Gregory) de Vries. Res. Bull. Hokkaido Natl. Agric. Exp. Stn. 1987, 148, 1–56. [Google Scholar]
  87. Panka, D.; Podkowka, L.; Lamparski, R. Preliminary observations on the resistance of meadow fescue (Festuca pratensis Huds.) infected by Neotyphodium uncinatum to diseases and pest and nutritive value. In Proceedings of the 5th International Symposium on Neotyphodium/ Grass Interactions, University of Arkansas, Fayetteville, AK, USA, 23–26 May 2004. [Google Scholar]
  88. Andrews, J.H. Biological control in the phyllosphere. Annu. Rev. Phytopathol. 1992, 30, 603–635. [Google Scholar] [CrossRef]
  89. Whitaker, B.K.; Bakker, M.G. Bacterial endophyte antagonism toward a fungal pathogen in vitro does not predict protection in live plant tissue. FEMS Microbiol. Ecol. 2018, 95, fiy237. [Google Scholar]
  90. Yakti, W.; Kovács, G.M.; Franken, P. Differential interaction of the dark septate endophyte Cadophora sp. and fungal pathogens in vitro and in planta. FEMS Microbiol. Ecol. 2019, 95, fiz164. [Google Scholar] [CrossRef]
  91. Blackenship, J.D.; Spiering, M.J.; Wilkinson, H.H.; Fannin, F.F.; Bush, L.P.; Schardl, C.L. Production of loline alkaloids by the grass endophyte, Neotyphodium uncinatum, in defined media. Phytochemistry 2001, 58, 395–401. [Google Scholar] [CrossRef]
  92. Spanu, P.D. The genomics of obligate (and nonobligate) biotrophs. Annu. Rev. Phytopathol. 2011, 50, 91–109. [Google Scholar] [CrossRef] [PubMed]
  93. Zabalgogeazcoa, I. Fungal endophytes and their interaction with plant pathogens. Span. J. Agric. Res. 2008, 6, 138–146. [Google Scholar] [CrossRef] [Green Version]
  94. De Kesel, J.; Conrath, U.; Flors, V.; Luna, E.; Mageroy, M.H.; Mauch-Mani, B.; Pastor, V.; Pozo, M.J.; Pieterse, C.M.; Ton, J. The induced resistance lexicon: Do’s and don’ts. Trends Plant Sci. 2021, 26, 685–691. [Google Scholar] [CrossRef]
  95. Viterbo, A.; Horwitz, B.A. Mycoparasitism. In Cellular and Molecular Biology of Filamentous Fungi; American Society for Microbiology Press: Washington, DC, USA, 2010; pp. 676–693. [Google Scholar]
  96. Christensen, M.J.; Zhang, X.; Scott, B. Regulation switching of Epichloe typhina within elongating perennial ryegrass leaves. Mycol. Res. 2008, 112, 1056–1062. [Google Scholar] [CrossRef] [PubMed]
  97. Christensen, M.J.; Bennett, R.J.; Ansari, H.A.; Koga, H.; Johnson, R.D.; Bryan, G.T.; Simpson, W.R.; Koolaard, J.P.; Nickless, E.M.; Voisey, C.R. Epichloë endophytes grow by intercalary hyphal extension in elongating grass leaves. Fungal Genet. Biol. 2008, 45, 84–93. [Google Scholar] [CrossRef]
  98. Yoshihara, T.; Togiya, S.; Koshino, H.; Sakamura, S.; Shimanuki, T.; Sato, T.; Tajimi, A. Three fungitoxic cyclopentanoid sesquiterpenes from stromata of Epichloe Typhina. Tetrahedron Lett. 1985, 26, 5551–5554. [Google Scholar] [CrossRef]
  99. Koshino, H.; Terada, S.-I.; Yoshihara, T.; Sakamura, S.; Shimanuki, T.; Sato, T.; Tajimi, A. Three phenolic acid derivatives from stromata of Epichloë typhina on Phleum Pratense. Phytochemistry 1988, 27, 1333–1338. [Google Scholar] [CrossRef]
  100. Koshino, H.; Togiya, S.; Yoshihara, T.; Sakamura, S.; Shimanuki, T.; Sato, T.; Tajimi, A. Four fungitoxic C-18 hydroxy unsaturated fatty acids from stromata of Epichloe Typhina. Tetrahedron Lett. 1987, 28, 73–76. [Google Scholar] [CrossRef]
  101. Koshino, H.; Yoshihara, T.; Sakamura, S.; Shimanuki, T.; Sato, T.; Tajimi, A. A ring B aromatic sterol from stromata of Epichloe Typhina. Phytochemistry 1989, 28, 771–772. [Google Scholar] [CrossRef]
  102. Bultman, T.L.; Leuchtmann, A. Biology of the Epichloë-Botanophila interaction: An intriguing association between fungi and insects. Fungal Biol. Rev. 2008, 22, 131–138. [Google Scholar] [CrossRef]
  103. Schiestl, F.P.; Steinbrunner, F.; Schulz, C.; von Reub, S.; Francke, W.; Weymuth, C.; Leuchtmann, A. Evolution of ‘pollinator’-attracting signals in fungi. Biol. Lett. 2006, 2, 401–404. [Google Scholar] [CrossRef]
  104. Koulman, A.; Lane, G.; Christensen, M.; Fraser, K.; Tapper, B.A. Peramine and other fungal alkaloids are exuded in the guttation fluid of endophyte-infected grasses. Phytochemistry 2007, 68, 355–360. [Google Scholar] [CrossRef]
  105. Pieterse, C.M.; van der Does, D.; Zamioudis, C.; Leon-Reyes, A.; van Wees, S.C. Hormonal modulation of plant immunity. Annu. Rev. Cell Dev. Biol. 2012, 28, 489–521. [Google Scholar] [CrossRef] [Green Version]
  106. Glazebrook, J. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu. Rev. Phytopathol. 2005, 43, 205–227. [Google Scholar] [CrossRef]
  107. Schmid, J.; Day, R.; Zhang, N.; Dupont, P.-Y.; Cox, M.P.; Schardl, C.L.; Minards, N.; Truglio, M.; Moore, N.; Harris, D.R. Host tissue environment directs activities of an Epichloë endophyte, while it induces systemic hormone and defense responses in its native perennial ryegrass host. Mol. Plant-Microbe Interact. 2017, 30, 138–149. [Google Scholar] [CrossRef] [Green Version]
  108. Moy, M.; Belanger, F.; Duncan, R.; Freehoff, A.; Leary, C.; Meyer, W.; Sullivan, R.; White, J.F., Jr. Identification of epiphyllous mycelial nets on leaves of grasses infected by clavicipitaceous endophytes. Symbiosis 2000, 28, 291–302. [Google Scholar]
  109. Tadych, M.; White, J. Ecology of epiphyllous stages of endophytes and implications for horizontal dissemination. NZGA Res. Pract. Ser. 2006, 13, 157–161. [Google Scholar] [CrossRef]
  110. Wang, H.; Sun, S.; Ge, W.; Zhao, L.; Hou, B.; Wang, K.; Lyu, Z.; Chen, L.; Xu, S.; Guo, J.; et al. Horizontal gene transfer of Fhb7 from fungus underlies Fusarium head blight resistance in wheat. Science 2020, 368, eaba5435. [Google Scholar] [CrossRef] [PubMed]
  111. Wulff, B.B.H.; Jones, J.D.G. Breeding a fungal gene into wheat. Science 2020, 368, 822. [Google Scholar] [CrossRef] [PubMed]
  112. Ambrose, K.V.; Belanger, F.C. SOLiD-SAGE of endophyte-infected red fescue reveals numerous effects on host transcriptome and an abundance of highly expressed fungal secreted proteins. PLoS ONE 2012, 7, e53214. [Google Scholar] [CrossRef] [Green Version]
  113. Wang, R.; Luo, S.; Clarke, B.B.; Belanger, F.C. The Epichloë festucae antifungal protein Efe-AfpA is also a possible effector protein required for the interaction of the fungus with its host grass Festuca rubra subsp. rubra. Microorganisms 2021, 9, 140. [Google Scholar] [CrossRef]
  114. Torres, M.; Singh, A.; Vorsa, N.; Gianfagna, T. Were endophytes pre-adapted for defensive mutualism? NZGA Res. Pract. Ser. 2006, 13, 63–67. [Google Scholar] [CrossRef]
  115. Xu, X.; Jeger, M. More ecological research needed for effective biocontrol of plant pathogens. In How Research Can Stimulate the Development of Commercial Biological Control Against Plant Diseases; Springer: Berlin/Heidelberg, Germany, 2020; pp. 15–30. [Google Scholar]
  116. Kuldau, G.; Bacon, C. Clavicipitaceous endophytes: Their ability to enhance resistance of grasses to multiple stresses. Biol. Control 2008, 46, 57–71. [Google Scholar] [CrossRef]
  117. Glare, T.; Caradus, J.; Gelernter, W.; Jackson, T.; Keyhani, N.; Köhl, J.; Marrone, P.; Morin, L.; Stewart, A. Have biopesticides come of age? Trends Biotechnol. 2012, 30, 250–258. [Google Scholar] [CrossRef] [PubMed]
  118. Schardl, C.L.; Craven, K.D.; Speakman, S.; Stromberg, A.; Lindstrom, A.; Yoshida, R. A novel test for host-symbiont codivergence indicates ancient origin of fungal endophytes in grasses. Syst. Biol. 2008, 57, 483–498. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  119. Popay, A.J.; Bonos, S.A. Biotic responses in endophytic grasses. In Neotyphodium in Cool-Season Grasses; Roberts, C.A., Charles, C.P., Spiers, D.E., Eds.; Blackwell Publishing: Ames, IA, USA, 2005; pp. 163–185. [Google Scholar]
  120. Bultman, T.L.; Aguilera, A.; Sullivan, T.J. Influence of fungal isolates infecting tall fescue on multitrophic interactions. Fungal Ecol. 2012, 5, 372–378. [Google Scholar] [CrossRef]
  121. Omacini, M.; Chaneton, E.J.; Ghersa, C.M.; Müller, C.B. Symbiotic fungal endophytes control insect host–parasite interaction webs. Nature 2001, 409, 78–81. [Google Scholar] [CrossRef]
  122. Fuchs, B.; Krischke, M.; Mueller, M.J.; Krauss, J. Peramine and lolitrem B from endophyte-grass associations cascade up the food chain. J. Chem. Ecol. 2013, 39, 1385–1389. [Google Scholar] [CrossRef]
  123. Casas, C.; Torretta, J.P.; Exeler, N.; Omacini, M. What happens next? Legacy effects induced by grazing and grass-endophyte symbiosis on thistle plants and their floral visitors. Plant Soil 2016, 405, 211–229. [Google Scholar] [CrossRef]
  124. Roberts, E.L.; Ferraro, A. Rhizosphere microbiome selection by Epichloë endophytes of Festuca Arundinacea. Plant Soil 2015, 396, 229–239. [Google Scholar] [CrossRef]
  125. Zhong, R.; Xia, C.; Ju, Y.; Li, N.; Zhang, X.; Nan, Z.; Christensen, M.J. Effects of Epichloë gansuensis on root-associated fungal communities of Achnatherum inebrians under different growth conditions. Fungal Ecol. 2018, 31, 29–36. [Google Scholar] [CrossRef]
  126. Mormile, B.W. Influence of Seed Microbiome on Fitness of Epichloë Infected Tall Fescue Seedlings. Master’s Thesis, Southern Connecticut State University, New Haven, CT, USA, 2016. [Google Scholar]
  127. Ju, Y.; Zhong, R.; Christensen, M.J.; Zhang, X. Effects of Epichloë gansuensis endophyte on the root and rhizosphere soil bacteria of Achnatherum inebrians under different moisture conditions. Front. Microbiol. 2020, 11, 747. [Google Scholar] [CrossRef]
  128. 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] [Green Version]
  129. Pozo, M.J.; López-Ráez, J.A.; Azcón-Aguilar, C.; García-Garrido, J.M. Phytohormones as integrators of environmental signals in the regulation of mycorrhizal symbioses. New Phytol. 2015, 205, 1431–1436. [Google Scholar] [CrossRef]
  130. Vignale, M.V.; Iannone, L.J.; Novas, M.V. Epichloë endophytes of a wild grass promote mycorrhizal colonization of neighbor grasses. Fungal Ecol. 2020, 45, 100916. [Google Scholar] [CrossRef]
  131. 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]
  132. Chu-Chou, M.; Guo, B.; An, Z.-Q.; Hendrix, J.; Ferriss, R.; Siegel, M.; Dougherty, C.; Burrus, P. Suppression of mycorrhizal fungi in fescue by the Acremonium coenophialum endophyte. Soil Biol. Biochem. 1992, 24, 633–637. [Google Scholar] [CrossRef]
  133. 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]
  134. Mack, K.M.; Rudgers, J.A. Balancing multiple mutualists: Asymmetric interactions among plants, arbuscular mycorrhizal fungi, and fungal endophytes. Oikos 2008, 17, 310–320. [Google Scholar] [CrossRef]
  135. Müller, J. Artificial infection by endophytes affects growth and mycorrhizal colonisation of Lolium Perenne. Funct. Plant Biol. 2003, 30, 419–424. [Google Scholar] [CrossRef]
  136. 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]
  137. Novas, M.V.; Iannone, L.J.; Godeas, A.M.; Cabral, D. Positive association between mycorrhiza and foliar endophytes in Poa bonariensis, a native grass. Mycol. Prog. 2009, 8, 75. [Google Scholar] [CrossRef]
  138. Omacini, M.; Eggers, T.; Bonkowski, M.; Gange, A.; Jones, T. Leaf endophytes affect mycorrhizal status and growth of co-infected and neighbouring plants. Funct. Ecol. 2006, 20, 226–232. [Google Scholar] [CrossRef]
  139. Vignale, M.V.; Iannone, L.J.; Scervino, J.M.; Novas, M.V. Epichloë exudates promote in vitro and in vivo arbuscular mycorrhizal fungi development and plant growth. Plant Soil 2018, 422, 267–281. [Google Scholar] [CrossRef]
  140. Vignale, M.V.; Iannone, L.J.; Pinget, A.D.; de Battista, J.P.; Novas, M.V. Effect of epichloid endophytes and soil fertilization on arbuscular mycorrhizal colonization of a wild grass. Plant Soil 2016, 405, 279–287. [Google Scholar] [CrossRef]
  141. 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]
  142. 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]
  143. Bastías, D.A.; Jauregui, R.; Applegate, E.R.; Altermann, E.; Card, S.D.; Johnson, L.J. Complete genome sequence of Paenibacillus sp. strain E222, a bacterial symbiont of an Epichloë fungal endophyte of ryegrass. Microbiol. Resour. Announc. 2020, 9, e00786-20. [Google Scholar] [CrossRef] [PubMed]
  144. Bastías, D.A.; Johnson, L.J.; Card, S.D. Symbiotic bacteria of plant-associated fungi: Friends or foes? Curr. Opin. Plant Biol. 2020, 56, 1–8. [Google Scholar] [CrossRef]
  145. Partida-Martinez, L.P.; de Looß, C.F.; Ishida, K.; Ishida, M.; Roth, M.; Buder, K.; Hertweck, C. Rhizonin, the first mycotoxin isolated from the zygomycota, is not a fungal metabolite but is produced by bacterial endosymbionts. Appl. Environ. Microbiol. 2007, 73, 793–797. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  146. Hoffman, M.T.; Gunatilaka, M.K.; Wijeratne, K.; Gunatilaka, L.; Arnold, A.E. Endohyphal bacterium enhances production of indole-3-acetic acid by a foliar fungal endophyte. PLoS ONE 2013, 8, e73132. [Google Scholar]
  147. Tudzynski, B.; Sharon, A. Biosynthesis, biological role and application of fungal phytohormones. In Industrial Applications; Springer: Berlin/Heidelberg, Germany, 2002; pp. 183–211. [Google Scholar]
  148. Sharaf, E.F.; Farrag, A.A. Induced resistance in tomato plants by IAA against Fusarium Oxysporum Lycopersici. Pol. J. Microbiol. 2004, 53, 111. [Google Scholar] [PubMed]
  149. Romo, M.; Leuchtmann, A.; García, B.; Zabalgogeazcoa, I. A totivirus infecting the mutualistic fungal endophyte Epichloë Festucae. Virus Res. 2007, 124, 38–43. [Google Scholar] [CrossRef] [PubMed]
  150. Zabalgogeazcoa, I.; Benito, E.P.; Ciudad, A.G.; Criado, B.G.; Eslava, A.P. Double-stranded RNA and virus-like particles in the grass endophyte Epichloë Festucae. Mycol. Res. 1998, 102, 914–918. [Google Scholar] [CrossRef]
  151. Petisco, C.; Garcia-Criado, B.; Zabalgogeazcoa, I.; Vázquez-de-Aldana, B.R. A spectroscopy approach to the study of virus infection in the endophytic fungus Epichloë festucae. Virol. J. 2011, 8, 1–9. [Google Scholar] [CrossRef] [Green Version]
  152. Burdon, J.J.; Zhan, J. Climate change and disease in plant communities. PLoS Biol. 2020, 18, e3000949. [Google Scholar] [CrossRef] [PubMed]
  153. Martinelli, F.; Scalenghe, R.; Davino, S.; Panno, S.; Scuderi, G.; Ruisi, P.; Villa, P.; Stroppiana, D.; Boschetti, M.; Goulart, L.R. Advanced methods of plant disease detection. A review. Agron. Sustain. Dev. 2015, 35, 1–25. [Google Scholar] [CrossRef] [Green Version]
  154. Kocmánková, E.; Trnka, M.; Juroch, J.; Dubrovský, M.; Semerádová, D.; Možný, M.; Žalud, Z. Impact of climate change on the occurrence and activity of harmful organisms. Plant Prot. Sci. 2009, 45, S48. [Google Scholar] [CrossRef] [Green Version]
  155. Misra, A.; Yadav, S.; Mishra, S.; Tripathi, M. Impact of meteorological variables and climate change on plant diseases. In Plant Pathogens; Apple Academic Press: Palm Bay, FL, USA, 2020; pp. 313–327. [Google Scholar]
  156. Yáñez-López, R.; Torres-Pacheco, I.; Guevara-González, R.G.; Hernández-Zul, M.I.; Quijano-Carranza, J.A.; Rico-García, E. The effect of climate change on plant diseases. Afr. J. Biotechnol. 2012, 11, 2417–2428. [Google Scholar] [CrossRef]
  157. Hu, S.; Firestone, M.K.; Chapin, F.S., III. Soil microbial feedbacks to atmospheric CO2 enrichment. Trends Ecol. Evol. 1999, 14, 433–437. [Google Scholar] [CrossRef]
  158. Hunt, M.G.; Rasmussen, S.; Newton, P.C.; Parsons, A.J.; Newman, J.A. Near-term impacts of elevated CO2, nitrogen and fungal endophyte-infection on Lolium perenne L. growth, chemical composition and alkaloid production. Plant Cell Environ. 2005, 28, 1345–1354. [Google Scholar] [CrossRef]
  159. Ueno, A.C.; Gundel, P.E.; Ghersa, C.M.; Demkura, P.V.; Card, S.D.; Mace, W.J.; Martínez-Ghersa, M.A. Ontogenetic and trans-generational dynamics of a vertically transmitted fungal symbiont in an annual host plant in ozone-polluted settings. Plant Cell Environ. 2020, 43, 2540–2550. [Google Scholar] [CrossRef]
  160. Pareek, A.; Dhankher, O.P.; Foyer, C.H. Mitigating the impact of climate change on plant productivity and ecosystem sustainability. J. Exp. Bot. 2020, 71, 451–456. [Google Scholar] [CrossRef]
  161. Qiu, J. Nitrogen Fertilizer Warning for China; Nature Publishing Group: Berlin, Germany, 2009. [Google Scholar]
  162. Dordas, C. Role of nutrients in controlling plant diseases in sustainable agriculture. A review. Agron. Sustain. Dev. 2008, 28, 33–46. [Google Scholar] [CrossRef] [Green Version]
  163. FAO. Special Event on Impact of Climate Change, Pests and Diseases on Food Security and Poverty Reduction. Background Document. In Proceedings of the 31st Session of the Committee on World Food Security, Rome, Italy, 13–16 April 2005. [Google Scholar]
  164. Philippot, L.; Raaijmakers, J.M.; Lemanceau, P.; van der Putten, W.H. Going back to the roots: The microbial ecology of the rhizosphere. Nat. Rev. Microbiol. 2013, 11, 789–799. [Google Scholar] [CrossRef] [PubMed]
  165. Card, S.D.; Faville, M.J.; Simpson, W.R.; Johnson, R.D.; Voisey, C.R.; de Bonth, A.C.; Hume, D.E. Mutualistic fungal endophytes in the Triticeae–survey and description. FEMS Microbiol. Ecol. 2014, 88, 94–106. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  166. Simpson, W.R.; Faville, M.J.; Moraga, R.A.; Williams, W.M.; Mcmanus, M.T.; Johnson, R.D. Epichloë fungal endophytes and the formation of synthetic symbioses in Hordeeae (= Triticeae) grasses. J. Syst. Evol. 2014, 52, 794–806. [Google Scholar] [CrossRef]
  167. Simpson, W.R. Hordeeae Epichloë endophytes and the formation of synthetic symbioses with cereal grasses. Ph.D. Thesis, Massey University, Palmerston North, New Zealand, 2016. [Google Scholar]
  168. Li, C.; Wang, Z.; Chen, T.; Nan, Z. Creation of novel barley germplasm using an Epichloë endophyte. Chin. Sci. Bull. 2021, 66, 2608. [Google Scholar] [CrossRef]
  169. O’Hanlon, K.A.; Knorr, K.; Jørgensen, L.N.; Nicolaisen, M.; Boelt, B. Exploring the potential of symbiotic fungal endophytes in cereal disease suppression. Biol. Control 2012, 63, 69–78. [Google Scholar] [CrossRef]
  170. Lewis, J.A.; Papavizas, G.C. Biocontrol of plant diseases: The approach for tomorrow. Crop Prot. 1991, 10, 95–105. [Google Scholar] [CrossRef]
  171. Card, S.; Johnson, L.; Teasdale, S.; Caradus, J. Deciphering endophyte behaviour: The link between endophyte biology and efficacious biological control agents. FEMS Microbiol. Ecol. 2016, 92. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  172. Bryant, R.H.; Cameron, N.E.; Edwards, G.R. Response of black beetle and redheaded pasture cockchafer larvae to loline alkaloids in meadow fescue roots. N. Z. Plant Prot. 2010, 63, 219–223. [Google Scholar] [CrossRef] [Green Version]
  173. Rostás, M.; Cripps, M.G.; Silcock, P. Aboveground endophyte affects root volatile emission and host plant selection of a belowground insect. Oecologia 2015, 177, 487–497. [Google Scholar] [CrossRef] [PubMed]
  174. Qawasmeh, A.; Raman, A.; Wheatley, W. Volatiles in perennial ryegrass infected with strains of endophytic fungus: Impact on African black beetle host selection. J. Appl. Entomol. 2015, 139, 94–104. [Google Scholar] [CrossRef]
  175. Swadling, I.R.; Jeffries, P. Isolation of microbial antagonists for biocontrol of grey mould disease of strawberries. Biocontrol Sci. Technol. 1996, 6, 125–136. [Google Scholar] [CrossRef]
Table
Table 1. In vitro bioactivity exhibited by species of Epichloë towards fungal saprophytes or phytopathogens. Bioassays reviewed here are generally dual culture assays using viable fungal colonies, or their filtered crude extracts, undertaken on potato dextrose agar (PDA) or a similar solid agar medium. These in vitro bioassays are restricted to only assessing antibiosis and cannot assess other mechanisms of action (i.e., induced resistance or competition).
Table 1. In vitro bioactivity exhibited by species of Epichloë towards fungal saprophytes or phytopathogens. Bioassays reviewed here are generally dual culture assays using viable fungal colonies, or their filtered crude extracts, undertaken on potato dextrose agar (PDA) or a similar solid agar medium. These in vitro bioassays are restricted to only assessing antibiosis and cannot assess other mechanisms of action (i.e., induced resistance or competition).
Fungal Species 1Host SpeciesFungal Pathogen 2DivisionCountryReference/s
Epichloë amarillansAchnatherum sibiricumCochliobolus lunatus (syn. Curvularia lunata)AscomycotaChina[37]
Cladosporium cucumeriumAscomycotaChina[37]
Fusarium oxysporumAscomycotaChina[37]
Phomopsis vexansAscomycotaChina[37]
Rhizoctonia solaniBasidiomycotaChina[37]
Agrostis sp. Cryphonectria parasiticaAscomycotaUSA[45]
Epichloë bromicolaHordeum brevisubulatumAlternaria sp.AscomycotaChina[46]
Epichloë chisosaAchnatherum sibiricumCochliobolus lunatus (syn. Curvularia lunata)AscomycotaChina[37]
Cladosporium cucumeriumAscomycotaChina[37]
Fusarium oxysporumAscomycotaChina[37]
Phomopsis vexansAscomycotaChina[37]
Rhizoctonia solaniBasidiomycotaChina[37]
Epichloë coenophialum (FaTG-1)Lolium arundinaceumAlternaria alternataAscomycotaUSA[47]
Ceratobasidium cornigerum (syn. Rhizoctonia cerealis)BasidiomycotaNZ and USA [40,48]
Cladosporium cladosporioidesAscomycotaUSA[47]
Cochliobolus lunatus (syn. Curvularia lunata)AscomycotaPoland[49]
Cochliobolus sativus (syn. Bipolaris sorokiniana)AscomycotaChina and Poland[49,50]
Cryphonectria parasiticaAscomycotaUSA[45]
Glomerella graminicola (syn. Colletotrichum graminicola)AscomycotaNZ and USA[40]
Laetisaria roseipellis (syn. Limonomyces roseipellis)BasidiomycotaNZ and USA[40]
Pyrenophora erythrospila (syn. Drechslera erythrospila)AscomycotaNZ and USA[41,51]
Gibberella acuminata (syn. Fusarium acuminatum)AscomycotaChina[50]
Rhizoctonia solaniBasidiomycotaPoland[49]
Waitea circinate (syn. Rhizoctonia zeae)BasidiomycotaNZ and USA[40]
Epichloë FaTG-2Lolium arundinaceumPyrenophora erythrospila (syn. Drechslera erythrospila)AscomycotaNZ[41]
Waitea circinate (syn. Rhizoctonia zeae)BasidiomycotaNZ[41]
Epichloë FaTG-3Lolium arundinaceumCeratobasidium sp.BasidiomycotaAustralia[52]
Drechslera sp.AscomycotaAustralia[52]
Pyrenophora erythrospila (syn. Drechslera erythrospila)AscomycotaNZ[41]
Waitea circinate (syn. Rhizoctonia zeae)BasidiomycotaNZ[41]
Epichloë festucaeFestuca longifoliaCeratobasidium cornigerum (syn. Rhizoctonia cerealis)BasidiomycotaNZ and USA[40]
Glomerella graminicola (syn. Colletotrichum graminicola)AscomycotaNZ, Japan and USA[40,53]
Laetisaria roseipellis (syn. Limonomyces roseipellis)BasidiomycotaNZ and USA[40]
Pyrenophora erythrospila (syn. Drechslera erythrospila)AscomycotaNZ[41]
Waitea circinate (syn. Rhizoctonia zeae)BasidiomycotaNZ[41]
Festuca pulchellaBotrytis cinereaAscomycotaJapan[54]
Cochliobolus sativus (syn. Bipolaris sorokiniana)AscomycotaJapan[53]
Drechslera dictyoidesAscomycotaJapan[53]
Drechslera siccansAscomycotaJapan[53]
Glomerella graminicola (syn. Colletotrichum graminicola)AscomycotaJapan[53]
Pyrenophora erythrospila (syn. Drechslera erythrospila)AscomycotaJapan[53,54,55]
Phytophthora infestansOomycotaJapan[54]
Festuca rubra 3Clarireedia homoeocarpa (syn. Sclerotinia homoeocarpa)AscomycotaUSA[56]
Cochliobolus sativus (syn. Bipolaris sorokiniana)AscomycotaPoland[57]
Ceratobasidium cornigerum (syn. Rhizoctonia cerealis)BasidiomycotaNZ and USA[40]
Cryphonectria parasiticaAscomycotaUSA[45]
Drechslera dictyoidesAscomycotaPoland[57]
Glomerella graminicola (syn. Colletotrichum graminicola)AscomycotaNZ, Japan and USA[40,53]
Laetisaria roseipellis (syn. Limonomyces roseipellis)BasidiomycotaUSA[40]
Pyrenophora erythrospila (syn. Drechslera erythrospila)AscomycotaNZ[41]
Waitea circinate (syn. Rhizoctonia zeae)BasidiomycotaNZ[41]
Festuca trachyphyllaBotrytis cinereaAscomycotaJapan[54]
Pyrenophora erythrospilaAscomycotaJapan[54]
Phytophthora infestansOomycotaJapan[54]
Lolium pratenseGlomerella graminicola (syn. Colletotrichum graminicola)AscomycotaJapan[53]
Epichloë festucae var. lolii (=LpTG-1)Lolium perenneCeratobasidium cornigerum (syn. Rhizoctonia cerealis)BasidiomycotaNZ and USA[40,47,48]
Glomerella graminicola (syn. Colletotrichum graminicola)AscomycotaNZ and USA[40,58]
Ceratobasidium sp.BasidiomycotaAustralia[52]
Cryphonectria parasiticaAscomycotaUSA[45]
Drechslera anderseniiAscomycotaGermany[59]
Drechslera poaeAscomycotaGermany[59]
Drechslera siccansAscomycotaGermany[59]
Drechslera sp.AscomycotaAustralia[52]
Drechslera teresAscomycotaGermany[59]
Fusarium sp.AscomycotaAustralia[52]
Gibberella acuminata (Fusarium acuminatum)AscomycotaChina[50]
Pyrenophora erythrospila (syn. Drechslera erythrospila)AscomycotaNZ[41]
Waitea circinate (syn. Rhizoctonia zeae)BasidiomycotaNZ and USA[40,41]
Laetisaria roseipellis (syn. Limonomyces roseipellis)BasidiomycotaNZ and USA[40]
Epichloë gansuensisAchnatherum inebriansAlternaria alternataAscomycotaChina[50]
Cochliobolus lunatus (syn. Curvularia lunata)AscomycotaChina[50]
Cochliobolus sativus (syn. Bipolaris sorokiniana)AscomycotaChina[50]
Gibberella acuminata (syn. Fusarium acuminatum)AscomycotaChina[50]
Epichloë hybrida (=LpTG-2)Lolium perennePyrenophora erythrospila (syn. Drechslera erythrospila)AscomycotaNZ[41]
Waitea circinate (syn. Rhizoctonia zeae)BasidiomycotaNZ[41]
Epichloë LpTG-3Lolium perenneCeratobasidium sp.BasidiomycotaAustralia[52]
Drechslera sp.AscomycotaAustralia[52]
Fusarium sp.AscomycotaAustralia[52]
Epichloë occultansLolium multiflorumGibberella acuminata (syn. Fusarium acuminatum)AscomycotaArgentina[60] *
Rhizoctonia solaniBasidiomycotaArgentina[60] *
Unknown Epichloë spp. Festuca simensisAlternaria alternataAscomycotaChina [61]
Aspergillus nigerAscomycotaChina[62]
Cochliobolus sativus (syn. Bipolaris sorokiniana)AscomycotaChina [61,62]
Cochliobolus lunatus (syn. Curvularia lunata)AscomycotaChina [61,62]
Festuca versutaCeratobasidium cornigerum (syn. Rhizoctonia cerealis)BasidiomycotaUSA[48]
Lolium perenneGlomerella graminicola (syn. Colletotrichum graminicola)AscomycotaNZ[58]
Pyrenophora erythrospila (syn. Drechslera erythrospila)AscomycotaNZ[58]
Poa amplaCryphonectria parasiticaAscomycotaUSA[45]
Poa autumnalisCryphonectria parasiticaAscomycotaUSA[45]
Poa interiorCryphonectria parasiticaAscomycotaUSA[45]
Poa palustrisCryphonectria parasiticaAscomycotaUSA[45]
Poa rigidifoliaCryphonectria parasiticaAscomycotaUSA[45]
Poa sp.Cryphonectria parasiticaAscomycotaUSA[45]
Poa sylvestrisCryphonectria parasiticaAscomycotaUSA[45]
Neotyphodium starii 4Festuca arizonicaGlomerella graminicola (syn. Colletotrichum graminicola)AscomycotaNZ[40]
Laetisaria roseipellis (syn. Limonomyces roseipellis)BasidiomycotaNZ and USA[40]
Waitea circinate (syn. Rhizoctonia zeae)BasidiomycotaNZ[40]
Festuca obtusaWaitea circinate (syn. Rhizoctonia zeae)BasidiomycotaNZ[40]
Epichloë tembladeraeFestuca argentinaCryphonectria parasiticaAscomycotaUSA[45]
Poa huecaCryphonectria parasiticaAscomycotaUSA[45]
Poa sp.Cryphonectria parasiticaAscomycotaUSA[45]
Epichloë uncinatumLolium pratense (syn. Festuca pratensis)Cochliobolus sativus (syn. Bipolaris sorokiniana)AscomycotaPoland[57]
Drechslera dictyoidesAscomycotaPoland[57]
Gibberella avenacea (Fusarium avenaceum)AscomycotaPoland[57]
Fusarium culmorumAscomycotaGermany[59]
Fusarium equisetiAscomycotaPoland[57]
Pyrenophora erythrospila (syn. Drechslera erythrospila)AscomycotaNZ[41]
Rhizoctonia solaniBasidiomycotaPoland[57]
Typhula ishikariensisBasidiomycotaFinland[63]
Waitea circinate (syn. Rhizoctonia zeae)BasidiomycotaNZ[41]
1 Current scientific name. 2 Current scientific name, or most accepted name, followed by the synonym used within the citing manuscript. 3 Including subspecies. 4 Nomen dubium according to [22]. * In vitro experiment with axenic cultures of the pathogen and grass seed infected with Epichloë.
Table
Table 2. In planta bioactivity exhibited by species of Epichloë towards fungal saprophytes or phytopathogens. In planta bioassays included all assays that did not work with axenic cultures of Epichloë spp. and included detached leaf assays, whole plant assays with plants grown in controlled climate rooms, glasshouses, or field trials. IR = induced resistance.
Table 2. In planta bioactivity exhibited by species of Epichloë towards fungal saprophytes or phytopathogens. In planta bioassays included all assays that did not work with axenic cultures of Epichloë spp. and included detached leaf assays, whole plant assays with plants grown in controlled climate rooms, glasshouses, or field trials. IR = induced resistance.
Fungal Species 1Original Host SpeciesType of AssociationFungal Pathogen 2DivisionDiseaseSuggested MechanismCountryReference/s
Epichloë bromicolaLeymus chinensisoriginalCochliobolus lunatus (syn. Curvularia lunata)AscomycotaCurvularia blightIRChina[64]
Cochliobolus sativus (syn. Bipolaris sorokiniana)AscomycotaSpot blotch and root rotIRChina[64]
originalWaitea circinate (syn. Rhizoctonia zeae)BasidiomycotaSheath and leaf spotIRPoland[49]
Secale cerealenovelCercosporidium graminisAscomycotaLeaf streakUnknownNZ[65]
novelPuccinia reconditaBasidiomycotaLeaf rustUnknownNZ[65]
Epichloë coenophialumLolium arundinaceumoriginalCochliobolus lunatus (syn. Curvularia lunata)AscomycotaCurvularia blightCompetition for nutrientsChina[66]
Epichloë festucaeFestuca rubraoriginalCochliobolus sativus (syn. Bipolaris sorokiniana)AscomycotaSpot blotch and root rotAntibiosisPoland[57]
originalDreschslera sp.AscomycotaHead blightAntibiosisPoland[57]
originalFusarium poaeAscomycotaHead blightAntibiosisPoland[57]
Festuca rubra L. subsp. rubranovelLaetisaria fuciformisBasidiomycotaRed threadCompetitive exclusionUSA[67]
Lolium perennenovelPyrenophora erythrospila (syn. Drechslera erythrospila)AscomycotaRed leaf spotAntibiosisJapan[53]
Epichloë festucae var. lolii (=LpTG-1)Lolium perenneoriginalAlternaria alternataAscomycotaLeaf spotIRChina[38]
originalCochliobolus lunatus (syn. Curvularia lunata)AscomycotaCurvularia blightIRChina[38]
originalCochliobolus sativus (syn. Bipolaris sorokiniana)AscomycotaSpot blotch and root rotAntibiosis, competition and/or IRChina[38,68,69]
originalFusarium chlamydosporumAscomycotaWiltIR
originalFusarium oxysporumAscomycotaFusarium wiltIRChina[38]
originalFusarium poaeAscomycotaHead blightIRPoland[70]
originalFusarium solaniAscomycotaSoft root rotIRChina[38]
originalGibberella acuminata (syn. Fusarium acuminatum)AscomycotaRoot rotIRChina[38]
originalPuccinia coronataBasidiomycotaCrown rustUnknownAustralia and China[71,72]
novelPyrenophora semeniperdaAscomycotaLeaf spotsAntibiosisAustralia[73]
Epichloë gansuensisAchnatherum inebriansoriginalAscochyta leptosporaAscomycotaAscochyta leaf blightAntibiosisChina[50]
originalAlternaria alternataAscomycotaLeaf spotAntibiosisChina[50]
originalBlumeria graminisAscomycotaPowdery mildewIRChina[74,75,76,77]
originalClaviceps purpureaAscomycotaErgotIRChina[78]
originalClonostachys roseaAscomycotaUnknownAntibiosisChina[50]
originalCochliobolus lunatus (syn. Curvularia lunata)AscomycotaCurvularia blightAntibiosisChina [50,79]
originalFusarium chlamydosporumAscomycotaWiltAntibiosisChina[50]
originalFusarium oxysporumAscomycotaFusarium wiltAntibiosisChina[50]
originalFusarium solaniAscomycotaSoft root rotAntibiosisChina[50]
originalGibberella acuminata (syn. Fusarium acuminatum)AscomycotaRoot rotAntibiosisChina[50]
originalGibberella avenacea (Fusarium avenaceum)AscomycotaFusarium head blightAntibiosisChina[50]
originalFusarium solaniAscomycotaSoft root rotAntibiosisChina[50]
Achnatherum sibiricumoriginalCochliobolus lunatus (syn. Curvularia lunata)AscomycotaCurvularia blightIRChina[79]
Achnatherum sibiricumoriginalErysiphalesAscomycotaPowdery mildewIRChina[79]
Epichloë occultansLolium multiflorumoriginalClaviceps purpureaAscomycotaErgotVector exclusionArgentina[80]
Epichloë sibiricumAchnatherum sibiricumoriginalCochliobolus lunatus (syn. Curvularia lunata)AscomycotaCurvularia blightIRChina[79]
Achnatherum sibiricumoriginalErysiphalesAscomycotaPowdery mildewIRChina[79]
Epichloë sinensisFestuca sinensisoriginalAlternaria alternataAscomycotaLeaf spotUnknownChina[81]
Epichloë sp.Bromus auleticusoriginalUstilago bullataBasidiomycotaHead smutUnknownArgentina[82]
Festuca sinensisoriginalAlternaria alternataAscomycotaLeaf spotAntibiosisChina [61]
originalGibberella acuminata (syn. Fusarium acuminatum)AscomycotaRoot rotAntibiosisChina[61]
originalCochliobolus sativus (syn. Bipolaris sorokiniana)AscomycotaSpot blotch and root rotAntibiosisChina [61]
originalCochliobolus lunatus (syn. Curvularia lunata)AscomycotaCurvularia blightAntibiosisChina [61]
Lolium arundinaceumoriginal wild grass and cultivarRhynchosporium sp.AscomycotaLeaf blotchAntibiosis, IR and/or improved host fitnessFinland[83]
Lolium perenneoriginalDrechslera siccansAscomycotaBrown blightIRPoland[84]
original Fusarium spp.AscomycotaFusarium blightIRPoland[84]
Epichloë typhinaPhleum pratenseoriginalCladosporium phleiAscomycotaPurple leaf spotUnknownJapan[85,86]
Epichloë uncinatumLolium pratense (syn. Festuca pratensis)originalCochliobolus sativus (syn. Bipolaris sorokiniana)AscomycotaSpot blotch and root rotAntibiosisPoland[57]
originalDreschslera sp.AscomycotaHead blightAntibiosisPoland[57]
originalFusarium poaeAscomycotaHead blightAntibiosisPoland[57]
originalPuccinia coronataBasidiomycotaCrown rustUnknownPoland[87]
1 Current scientific name. 2 Current scientific name, or most accepted name, followed by the synonym used within the citing manuscript.
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Card, S.D.; Bastías, D.A.; Caradus, J.R. Antagonism to Plant Pathogens by Epichloë Fungal Endophytes—A Review. Plants 2021, 10, 1997. https://doi.org/10.3390/plants10101997

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Card SD, Bastías DA, Caradus JR. Antagonism to Plant Pathogens by Epichloë Fungal Endophytes—A Review. Plants. 2021; 10(10):1997. https://doi.org/10.3390/plants10101997

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Card, Stuart D., Daniel A. Bastías, and John R. Caradus. 2021. "Antagonism to Plant Pathogens by Epichloë Fungal Endophytes—A Review" Plants 10, no. 10: 1997. https://doi.org/10.3390/plants10101997

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