Asexual Epichloë Fungi—Obligate Mutualists: Comparison
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Asexual Epichloë are obligate fungal mutualists that form symbiosis with many temperate grass species, providing several advantages to the host. These advantages include protection against vertebrate and invertebrate herbivores (i.e., grazing livestock and invertebrate pests, respectively), improved resistance to phytopathogens, increased adaptation to drought stress, nutrient deficiency, and heavy metal-containing soils. Selected Epichloë strains are utilised in agriculture mainly for their pest resistance traits, which are moderated via the production of Epichloë-derived secondary metabolites. For pastoral agriculture, the use of these endophyte infected grasses requires the balancing of protection against insect pests with reduced impacts on animal health and welfare.

  • alkaloids
  • animal toxicosis
  • biocontrol
  • endophyte
  • fescue
  • ryegrass

1. History

Microbial endophytes, primarily comprising archaea, bacteria, fungi, or viruses, are associated with most plant species [1][2]. The term ‘endophyte’ was derived from the Greek words ‘endon’ (within) and ‘phyton’ (plant) [3], and initially included both pathogenic and beneficial microorganisms [4]. However, the term endophyte has now become synonymous with mutualism in reference to microbes that spend all or part of their life cycle within the plant host while causing no apparent disease symptoms [5][6], and provides a net benefit outcome to both itself and the host plant [7].

Asexual Epichloë endophytes (previously belonging to the taxonomic genus Neotyphodium [8]) were identified in the 1980/90s as the cause of two economically important diseases that affected livestock that grazed fescue in the USA and perennial ryegrass in New Zealand, namely fescue toxicosis [9] and ryegrass staggers [10], respectively (Figure 1). These obligate symbionts are mutualistic, relying on the host plant for their growth, survival, and transmission through hyphal colonisation of the host’s seed [11]. These endophytes exhibit a degree of host-specificity within the cool-season grasses of the Pooideae, whereby Epichloë species are naturally restricted to a host grass genus or closely related genera within a grass tribe [12][13][14]. Asexual Epichloë spend their entire life cycle within the plant host growing systemically within shoot tissues between plant cells [15][16][17] (Figure 2). However, their bioactivity towards certain pests in the rhizosphere [18] can be attributed to the mobility of fungal secondary metabolites in the roots, produced during the symbiosis, within the plant vascular system [15][16].

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Figure 1. Animal ailments caused by some Epichloë secondary metabolites: (a) ryegrass staggers caused by lolitrem B, and (b) fescue toxicosis caused by ergovaline; (c) fecal soiling in the breech area (‘dags’) of sheep exacerbated, on left, by a combination of secondary metabolites. (Images (a) and (c) courtesy of L. Fletcher; image (b) courtesy of J. Bouton).
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Figure 2. Epichloë hyphae, (a) stained with aniline blue (bar top right is 20µm) (image courtesy of W. Zhang), and (b) shown in a transmission electron micrograph growing between leaf cells with the hyphae labelled H (image courtesy of W. Zhang); and (c) a cross section of a grass tiller showing hyphae of a strain modified to express green fluorescent protein (image courtesy of M. Christensen).

Epichloë-derived secondary metabolites protect the host plant from herbivores—both vertebrates and invertebrates. However, the effect on ruminants and several non-ruminants including horses, camels, white rhinoceros, and alpacas [19] can be detrimental and, when first discovered, removal of these endophytes from grasses was considered the best solution. However, in many temperate regions of the world, such as New Zealand, these Epichloë endophytes are essential for pasture persistence. Novel endophyte strains have now been identified and commercialised that provide the host grass with tolerance/resistance to pests, diseases, and some abiotic stresses while reducing or eliminating the debilitating animal health and welfare issues [20]. These endophytes can be transferred between plants through artificial infection [21].

2. Epichloë Endophytes—A Necessity for the Pastoral Industry?

2.1. Taxonomy and Distribution

Epichloë fungi are found in the Clavicipitaceae family [22]. As a result of taxonomists being required to have a single genus name for all stages of the development of a fungal species [23], the Epichloë genus contains both sexual (teleomorph) and asexual (anamorph) forms. The latter had previously been classified as Neotyphodium [8]. More than 100 cool-temperate grass species host Epichloë, with the majority originating from Europe and Asia, and with many fewer from Australasia, sub-Saharan Africa, and South America (Table 1).

Asexual Epichloë strains are either hybrid as a result of a cross between two or more species, or are non-hybrid [14][24]. While all hybrid types are asexual, those classified as non-hybrid types are also incapable of sexual reproduction [25][26]. Compared with other fungal genera, Epichloë has the greatest number of interspecific hybrids [27].

Table 1. Epichloë species found in different grass genera across a range of territories.
Grass Genus (Common Names)Epichloë SpeciesRegionReference
AchnatherumE. gansuensis, E. sibirica; E. chisosa; E. inebrians; E. funkiiAsia[8][24][28][29]
AgropyronE. bromicolaEurope/North Africa[30]
Agrostis (browntop)E. baconii, E. amarillansEurope/North Africa[31]
AmmophilaE. amarillansNorth America[32]
AnthoxanthumE. typhinaEurope/North Africa[31]
BrachyelytrumE. brachyelytriEurope/North Africa; North America[31][33]
BrachypodiumE. sylvatica; E. typhina; E. bromicolaEurope/North Africa; Asia[29][31]
BrizaE. tembladeraeSouth America[34]
BromusE. bromicola; E. cabralii; E. typhina subsp. poae var.aonikenkana ; E. typhina; E. tembladerae; E. pampeanaEurope/North Africa; Asia; North America; South America[8][29][31][34][35][36][37]
CalamagrostisE. stromatolongaAsia[29]
CinnaE. schardliiNorth America[38]
Dactylis (cocksfoot)E. typhinaEurope/North Africa[31]
DichelachneE. australiensisNew Zealand[39]
EchinopogonE. australiensis; E. aotearoaeAustralia; New Zealand[40][41]
ElymusE. elymi; E. bromicola; E. canadensisEurope/North Africa; Asia; North America[8][24][29][31][33][42]
ElytrigiaE. spp.Asia[29]
Festuca (fescue)E. coenophiala; E. festucae; E. uncinata; E. siegelii; E. sinofestucae; E. typhinum var. huerfana, E. tembladeraeEurope/North Africa; Asia; North America; South America[29][31][43][44][45]
GlyceriaE. glyceriaeEurope/North Africa; North America[31][33]
HolcusE. typhina subsp. clarkii; E. mollisEurope/North Africa[8][31][46]
HordelymusE. disjuncta, E. danica, E. hordelymi, E. sylvatica subsp. pollinensis,Europe/North Africa[8][26]
HordeumE. tembladerae, E. amarillans, E. typhina hybridsSouth America[47]
Lolium (ryegrass)E. occultans; E. typhina var. canariensis; E. hybrida; E. festucae var. lolii, E. typhina,Europe/North Africa[8][27][31][48]
LeymusE. bromicolaEurope/North Africa; Asia[29][31]
MelicaE. melicicola; E. guerinii; E. tembladeraeSouth America; Sub-Saharan Africa; South America[8][24][34][41]
Phleum (timothy)E. typhina; E. cabralii; E. tembladeraeEurope/North Africa; South America[8][31][34][37]
PoaE. typhina; E. liyangensis; E. alsodes; E. typhina subsp. poae; E. tembladerae; E. novae-zelandiaeEurope/North Africa; Asia; North America; South America; New Zealand[31][34][39][43][49]
RoegneriaE. sinica; E. bromicolaAsia[29][50]
SphenopholisE. amarillansEurope/North Africa[31]
StipaE. spp.Asia[29]

2.2. Life Cycle

In planta, asexual Epichloë spp. complete their entire life cycle within the host plant’s tissues (Figure 3). Dissemination of Epichloë to the next plant generation occurs through vertical transmission of fungal hyphae via the seed of the host plant [51] and is moderated by the compatibility of the endophyte strain with the host’s genetics. Asexual Epichloë generally do not produce spores except when grown axenically within a laboratory environment [52].

Figure 3. Schematic diagram of the asexual Epichloë endophytic life cycle in cool-season grasses of the Pooideae.

When used in managed pastoral ecosystems, viability of the endophyte in seed can be threatened if the seed is stored at ambient temperatures and humidity [53]. However, storage of seed with a moisture level below 8% at temperatures below 5 °C and relative humidity of less than 30% will ensure long term endophyte viability [54].

2.3. Secondary Metabolite Bioactivity and its Consequences

The impact of Epichloë in natural and agricultural ecosystems is largely driven by chemistry. The genome of the endophyte strain determines the types (quality) of secondary metabolites expressed, but the host plant genome largely regulates the amount (quantity) [55][56]. Considerable information is known about four types of these secondary metabolite compounds (Figure 4) [55][56][57]:

  1. Ergot alkaloids—can be divided into four groups based on their chemical structure: clavines (e.g., chanoclavine, agroclavine), lysergic acid, lysergic acid amides (e.g., ergonovine, ergine), and ergopeptines (e.g., ergovaline, ergotamine, ergocornine, ergocristine, ergosine, ergocryptine).
  2. Indole diterpenoids—lolitrems, epoxyjanthitrems, terpendoles, paxilline.
  3. Lolines—N-formyl loline (NFL), N-acetyl loline (NAL), N-acetylnorloline (NANL).
  4. Pyrrolopyrazine—peramine.

Figure 4. Molecular structures of the known secondary metabolites produced by Epichloë, in planta. Ergot alkaloids include chanoclavine, lysergic acid, ergine, and ergovaline; indole diterpenes include paxilline, terpendole I, lolitrem B, and epoxyjanthitrem II; peramine; and the lolines. (Figure provided courtesy of W. Mace).

Seasonal climatic effects can also have an overriding effect on the concentrations of secondary metabolites expressed [58][59][60]. These tend to be higher in the warmer drier periods of summer and autumn and lower through the cooler winter period (Figure 5).

Figure 5. Seasonal trends in expression of ergovaline (a), lolitrem B (b), and peramine (c). Red shaded area represents summer months for the Northern and Southern Hemisphere. Figures modified from Fuchs et al [61] and Watson et al [62].

Secondary metabolite distribution within the plant can vary with compounds and among host species. In ryegrass, ergovaline is concentrated in the stem and basal leaf sheath of intermediate aged tillers, lolitrem B accumulates in older tissues, and peramine is distributed evenly across all leaf tissues [63]. In meadow fescue, lolines are found in both shoot and root tissues [64].

The bioactive impacts of Epichloë strains can vary depending on the quality and quantity of secondary metabolites expressed. Secondary metabolites causing most of the negative effects on mammals have been elucidated, but research continues to understand the role of beneficial secondary metabolites that provide advantages to host plant persistence (Table 2).

Table 2. Bioactivity of asexual Epichloë endophyte in grasses.
Bioactivity TraitConsequenceCausationReferences
Disadvantageous bioactivity
Fescue toxicosisFescue foot, high core body temperature, increased respiration, low heart rate, altered fat metabolism, low serum prolactin, failure or reduced milk production produce milk, suppression of the immune system, reduced forage intake, low rate of weight gain, and reproductive problems.Ergot alkaloids[65][66][67]
Ryegrass staggersNeurotoxic disease with symptoms ranging from slight muscular tremors through to staggering, and collapse. Can be associated with animal deaths.Lolitrem B, other indole diterpenoids; sub-chronic threshold of 1.55 ppm for cattle and 2 to 2.5 ppm for sheep[68][69][70]
Heat stressAnimals that are exposed to high concentrations of ergot alkaloids lose their ability to dissipate heat through restricted blood flow.Ergovaline and other ergot alkaloids[67][71][72]
Fecal soiling of the breech (dags)Leads to higher incidence of myiasis (flystrike).Ergovaline and lolitrem B[73]
Reduced animal performanceReduced liveweight gains and milk yields.Ergovaline and lolitrem B[73][74]
Ryegrass toxicosisCan result in death through misadventure.Documented only in Australia and likely to be a combination of ergot alkaloids and lolitrem B[75][76][77]
Equine fescue oedemaInappetence, depression, and subcutaneous oedema of the head, neck, chest, and abdomen in horses.Only noted with endophytes in Mediterranean-type tall fescues[78][79]
Reduced herbivore feedingDeterrence to feeding.Ergovaline and other ergot alkaloids[80][81][82]
Livestock toxicosis (Australia, New Zealand)Rare toxicosis in grazing livestock after Poa matthewsii and Echinopogon consumption.Possible paxilline[41][83]
Huecu toxicosis (Argentina)Intoxication in grazing animals after Poa and Festuca grazing infected with E. tembladerae.Indole-diterpenoid and ergot alkaloids[84][85]
Sleepy grass toxicosis (USA)Intoxication and narcosis in grazing livestock after Stipa robusta consumption.Lysergic acid amide[86][87]
Drunken horse grass toxicosis (Mongolia, China)Intoxication and narcosis in horses, donkeys, sheep, goats, and cattle after Achnatherum inebrians consumption.Ergot, ergonovine, lysergic acid, stipatoxin[88]
Dronkgras toxicosis (South Africa)Drunk-like behaviour of cattle, horses, donkeys consuming Melica decumbens.Indole-diterpenoids[89][90]
Advantageous bioactivity
Insect pest

resistance		Improved plant persistence and yield in presence of some insect pests.Various alkaloids depending on insect species (Table 3)[72][91][92]
Plant pathogen

resistances		Reduced incidence to some fungal diseases.Many known, but possible effects of peroxidase activity, phenolic compounds and antifungal proteins[72][93][94][95]
Drought (low water supply) toleranceImproved tolerance of drought through moderation of stomatal conductance, enhanced osmoregulation.Largely unknown, but compounds implicated include polyols; increased levels of sugars and proline[96][97][98][99][100][101][102][103]
AllelopathyEndophytic fescue plants reduce radicle elongation and growth of competing seedling species; but can detrimental on companion Trifolium species.Total phenolic compound concentration was greater in endophytic than non-endophytic plants[104]
Heavy metal toleranceImproved growth in presence of cadmium, nickel.Unknown; in case of cadmium improved translocation to shoot, but for nickel reduced translocation to shoot[105][106]
Aluminium toleranceAluminium sequestration was greater on root surfaces and in root tissues of endophytic plants.Increased exudation of phenolic-like compounds from roots of endophytic plants[107]
Salinity toleranceImproved leaf survival; changes of anatomical structures reducing water loss; and allowing water, nutrients, photosynthates translocation.Unknown, but decreased sodium potassium and chlorine uptake[108][109]
Nutrient uptakeIncreased uptake of N and P from low levels of supply.Unknown[96][98][110][111]

The mode of action of secondary metabolites against insect pests continues to be understood as new endophyte strains are discovered and improved control of insect pests is achieved (Table 3).

Table 3. Mode of action of Epichloë secondary metabolites against invertebrates.
Secondary MetaboliteMode of ActionInvertebrates AffectedReference
Ergot alkaloids
ErgovalineDeterrent; anti-feeding; toxicArgentine stem weevil (Listronotus bonariensis) adults; African black beetle (Heteronychus arator) adults; root aphid (Aploneura lentisci); Japanese beetle (Popillia japonica) larvae; black cutworm (Agrostis ipsilon); nematode (Pratylenchus scribneri)[112][113][114][115][116]
ErgocryptineDeterrent; anti-feeding; toxicArgentine stem weevil adults and larvae; fall armyworm (Spodoptera frugiperda) larvae; nematode (Pratylenchus scribneri)[117][118]
Indole diterpenoids
Lolitrem BDeterrent; anti-feedingArgentine stem weevil larvae; circumstantial effect on Paratylenchus nematode[119]
PaxillineDeterrent; anti-feedingArgentine stem weevil larvae[120]
EpoxyjanthitremsDeterrent and toxicPorina[121]
Lolines
N-formyl loline, N-acetyl loline, N-acetylnorlolineDeterrent; anti-feedingGrass grub (Costelytra giveni); horn flies (Haematobia irritans); African black beetle; field cricket (Gryllidae spp.); Japanese beetle (Popillia japonica) larvae[122][123][124][125]
Deterrent and toxicArgentine stem weevil larvae and adults; milkweed bug (Oncopeltus fasciatus); corn borer (Ostrinia nubilalis) larvae; aphid (Rhopalosiphum padi and Schizaphis graminum); fall armyworm (Spodoptera frugiperda) larvae; porina larvae (Wiseana ssp.); nematode (Pratylenchus scribneri)[126][127][128][129][130]
Pyrrolopyrazine
PeramineDeterrent; anti-feedingArgentine stem weevil adults and larvae[120][131]
Not a deterrent, but disrupted developmentCutworm (Graphania mutans)[118]

However, there are also many unidentified secondary metabolites that are known to exist through bioactivity against invertebrates that cannot be attributed to known chemistry. In addition, Epichloë endophytes boost the jasmonic acid pathway, which in turn, enhances the host plant’s immunity to chewing insects [132]. Grass emitted volatile organic compounds triggered by an aphid infestation can also be enhanced through Epichloë endophyte infection [133]. These volatiles have been shown to attract syrphid flies, which are natural enemies of aphids [134].

2.4. Application and Value to the Pastoral Industry

In a pastoral agriculture context, Epichloë endophytes are essential for temperate grass persistence in New Zealand, Australia, the USA, South America, and, to a lesser extent, Europe [135]. The absence of an Epichloë endophyte or use of an inappropriate strain can result in complete pasture loss, as shown in a comparative trial in the Waikato region of New Zealand (Figure 6). However, to ensure the disadvantageous impacts of Epichloë on animal health and welfare are minimised, strains of endophyte that do not express those secondary metabolites at levels causing these issues have been identified, isolated, and then re-inoculated into high yielding plant germplasm [72][136]. This has resulted in several novel Epichloë strain-host associations being commercialised [137][138][139][140][141][142]. Table 4 summarises the performance of these commercialised strains and their known chemistry.

Figure 6. The loss of persistence due to insect pests and drought on ryegrass with either no Epichloë endophyte or an ineffective strain on ryegrass persistence in the Waikato region of New Zealand.

Table 4. Summary of known chemistry, impacted insect pests, and animal performance of commercialised Epichloë endophyte strains (reviewed in Caradus et al [142]).
Epichloë Brand (or Strain)Known ChemistryInsect Pest Affects Significantly ReducedAnimal PerformanceReferences
Ryegrass; endophytes are E. festucae var lolii, or E. festucae
Nil endophyteNo chemistryNo insect pest protectionExcellent[74][81][143][144]
AR1PeramineArgentine stem weevil (larva), pasture mealybug (Balanococcus poae)Excellent[81]
AR37EpoxyjanthitremsArgentine stem weevil (adult), pasture mealybug, porina, African black beetle, root aphidExcellent, but minor staggers can occur with sheep/lambs[145]
NEA (NEA2)Low ergovaline and peramine, very low lolitrem BPasture mealybug, African black beetleExcellent[146][147]
NEA2 (mix of NEA2 and NEA6)Medium ergovaline, medium-low peramine, very low lolitrem BArgentine stem weevil, pasture mealybug, African black beetle, root aphidExcellent, but lamb live weight gain could be reduced in extreme circumstances[147][148][149][150][151]
NEA4 (mix of NEA2 and NEA3)Medium ergovaline, medium-low peramine, very low lolitrem BArgentine stem weevil, pasture mealybug, African black beetleExcellent, but lamb live weight gain could be reduced in extreme circumstances[147]
Standard endophyteHigh ergovaline, peramine and lolitrem BArgentine stem weevil, pasture mealybug, African black beetle; root aphidCan cause ryegrass staggers in sheep and lambs, and significantly decrease lamb growth rates in summer and autumn, and significantly increase dags.

In dairy cows, it has been shown to depress milksolids production through summer and autumn.		[74][81][143][144][149][151]
Festulolium; endophyte is E. uncinatum
U2Loline compounds NFL, NAL, and NANLAfrican black beetle, Argentine stem weevil, pasture mealybug, root aphid, grass grub, field cricketsExcellent[124][152][153]
Tall fescue; endophytes are E. coenophiala
Nil endophyteNo chemistryNo insect protectionExcellent[154]
MaxQ II (USA); MaxP (NZ, Australia) (AR584)Peramine, loline compounds NFL, NAL, and NANLAfrican black beetle, Argentine stem weevil, pasture mealybug, grass grub, root aphid, fall armyworm, corn flea beetle (Chaetocnema pulicaria), bird cherry-oat aphid (Rhopalosiphum padi), field cricketsExcellent[155][156]
E34Low ergovalineNot testedExcellent; lowered blood serum prolactin levels[156]

The economic benefit of some of the more widely commercialised strains has been estimated. For example, the value to the New Zealand economy from AR37 has been calculated to be NZ$3.6 billion over the 20-year life of its patent [157]. In the USA, the positive financial benefits of MaxQ tall fescue have been demonstrated for beef cows, calves, and feeder cattle farming systems [158][159] and sheep farming systems [160].

3. Epichloë Endophytes—Applications Outside the Pastoral Industry

3.1. Application to the Turf Industry

For grassed areas such as airports, children’s playgrounds, sports turf, and parks, which exclude domesticated grazing animals, Epichloë endophytes that produce deterrent secondary metabolites such as ergot alkaloids, lolitrem B, and lolines have been deliberately used to discourage herbivores such as rabbits, granivorous birds, and rodents [161][162][163][164][165].

3.2. Application to Cereals

While Epichloë endophytes are not naturally found in modern cereals such as wheat (Triticum aestivum), barley (Hordeum vulgare), oats (Avena sativa), or rye (Secale cereale), they are found in wild grasses related to these species, namely from the genera Elymus and Hordeum [166]. Research has set out to determine whether Epichloë can provide the same benefits to cereals as they do to temperate grasses. Artificial inoculation of Epichloë strains from wild grasses into wheat and rye can result in stunted or dwarf phenotypes due to compatibility issues [167]. However, in outbreeding rye, the range of phenotypes can result in normal phenotypes, which, in the field, provide the host plant with increased fungal pathogen resistance and improved yields under some managements [168], and reduce damage from a range of insect pests [169][170]. In wheat, inoculations have been possible through using Chinese spring wheat addition lines [171].

4. Conclusions and Prospects

The mutualistic relationship between asexual Epichloë spp. and cool-season grasses is critical for the maintenance of temperate grass based pastoral agriculture in several countries. While it remains more of a biological curiosity in Europe, where this mutualistic association evolved between Epichloë and the host species of Lolium and Festuca, it is essential in many countries where these grasses were introduced due to the prevalence of both introduced and endemic insect pests and pathogens, and the compounding effect of drought and heat [72][103]. Changes in climate, management, and further pest incursions will continue to challenge the persistence of cool-season grasses making the reliance on the mutualism with Epichloë even more important. The ongoing search for novel endophytes with beneficial chemistry continues, but can now be supplemented with the use of new techniques such as gene editing to design endophyte strains for specific biotic and abiotic challenges [172][173]. The ultimate outcome will be the delivery of natural biocontrol options to protect grasses from pest and disease challenges, without the use of synthetic chemistry, and improve yield in drought conditions.

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