Epichloë
"Choke disease":Epichloë typhina stroma onbluegrass
Scientific classification
Kingdom:	Fungi
Division:	Ascomycota
Class:	Sordariomycetes
Order:	Hypocreales
Family:	Clavicipitaceae
Tribe:	Balansiae
Genus:	Epichloë (Fr.)Tul. &C.Tul (1865)
Type species
Epichloë typhina (Fr.) Tul. & C.Tul. (1865)
Diversity
37 species, see text
Synonyms[1]
Cordyceps subgen.EpichloëFr. (1849) HyperdermiumJ.F. White, R.F. Sullivan, Bills & Hywel-Jones (2000) NeotyphodiumGlenn, C.W. Bacon & Hanlin (1996) TyphodiumLink (1826) [1824]

Epichloë is agenus ofascomycetefungi forming anendophyticsymbiosis withgrasses. Grasschoke disease is a symptom in grasses induced by someEpichloë species, which formspore-bearing mats (stromata) ontillers and suppress the development of theirhost plant'sinflorescence. For most of their life cycle however,Epichloë grow in the intercellular space of stems, leaves, inflorescences, and seeds of the grass plant without incurring symptoms of disease. In fact, they provide several benefits to their host, including the production of different herbivore-deterringalkaloids, increased stress resistance, and growth promotion.

Within the familyClavicipitaceae,Epichloë is embedded in a group of endophytic andplant pathogenic fungi, whose common ancestor probably derived from an animal pathogen. The genus includes both species with a sexually reproducing (teleomorphic) stage andasexual,anamorphic species. The latter were previously placed in theform genusNeotyphodium but included inEpichloë aftermolecular phylogenetics had shown asexual and sexual species to be intermingled in a singleclade.Hybrid speciation has played an important role in the evolution of the genus.

Epichloë species are ecologically significant through their effects on host plants. Their presence has been shown to alter the composition ofplant communities andfood webs. Grass varieties, especially oftall fescue andryegrass, with symbioticEpichloë endophyte strains, are commercialised and used forpasture andturf.

Elias Fries, in 1849, first definedEpichloë as asubgenus ofCordyceps.^[2] Astype species, he designatedCordyceps typhina,^[2] originally described byChristiaan Hendrik Persoon.^[3] The brothersCharles andLouis René Tulasne then raised the subgenus to genus rank in 1865.^[4]Epichloë typhina would remain the only species in the genus until the discovery of fungal grass endophytes causing livestock intoxications in the 1970s and 1980s, which stimulated the description of new species.^[5] Several species from Africa and Asia that develop stromata on grasses were split off as a separate genusParepichloe in 1998.^[6]

ManyEpichloë species have forms that reproduce sexually, and several purely asexual species are closely related to them. Theseanamorphs were long classified separately: Morgan-Jones and Gams (1982) collected them in a section (Albo-lanosa) of genusAcremonium.^[7] In amolecular phylogenetic study in 1996, Glenn and colleagues found the genus to bepolyphyletic and proposed a new genusNeotyphodium for the anamorphic species related toEpichloë.^[8] A number of species continued to be described in both genera until Leuchtmann and colleagues (2014) included most of theform genusNeotyphodium inEpichloë.^[5] Phylogenetic studies had shown both genera to be intermingled, and thenomenclatural code required since 2011 that one single name be used for all stages of development of a fungal species. OnlyNeotyphodium starrii, of unclear status, andN. chilense, which is unrelated, were excluded fromEpichloë.^[5]

As of 2024, there are 44 accepted species in the genus, with 1subspecies and 5varieties described. 20 species, 1 subspecies and 4 varieties are haploid. 24 species and 1 variety are hybrids (allopolyploids). Several taxa are only known as anamorphic (asexual) forms, most of which have previously been classified inNeotyphodium.^[5]

Epichloë species are specialized to form and maintain systemic, constitutive (long-term)symbioses with plants, often with limited or no disease incurred on the host.^[9] The best-studied of these symbionts are associated with thegrasses andsedges, in which they infect the leaves and other aerial tissues by growing between the plant cells (endophytic growth) or on the surface above or beneath the cuticle (epiphytic growth). An individual infected plant will generally bear only a single genetic individual clavicipitaceous symbiont, so the plant-fungus system constitutes a genetic unit called a symbiotum (pl. symbiota).

Symptoms and signs of the fungal infection, if manifested at all, only occur on a specific tissue or site of the hosttiller, where the fungal stroma or sclerotium emerges. The stroma (pl. stromata) is a mycelial cushion that gives rise first to asexual spores (conidia), then to the sexual fruiting bodies (ascocarps; perithecia).Sclerotia are hard resting structures that later (after incubation on the ground) germinate to form stipate stromata. Depending on the fungus species, the host tissues on which stromata or sclerotia are produced may be young inflorescences and surrounding leaves, individual florets, nodes, or small segments of the leaves. Young stromata are hyaline (colorless), and as they mature they turn dark gray, black, or yellow-orange. Mature stromata eject meiotically derived spores (ascospores), which are ejected into the atmosphere and initiate new plant infections (horizontal transmission). In some cases no stroma or sclerotium is produced, but the fungus infects seeds produced by the infected plant, and is therebytransmitted vertically to the next host generation. MostEpichloë species, and all asexual species, can vertically transmit.

The taxonomic dichotomy is especially interesting in this group of symbionts, because vegetative propagation of fungalmycelium occurs by vertical transmission, i.e., fungal growth into newly developing host tillers (=individual grass plants). Importantly, manyEpichloë species infect new grass plants solely by growing into the seeds of their grass hosts, and infecting the growing seedling.^[10][11] Manifestation of the sexual state — which only occurs inEpichloë species — causes "choke disease", a condition in which grassinflorescences are engulfed by rapid fungal outgrowth forming a stroma. The fungal stroma suppresses host seed production and culminates in the ejection of meiospores (ascospores) that mediate horizontal (contagious) transmission of the fungus to new plants.^[10] So, the two transmission modes exclude each other, although in many grass-Epichloë symbiota the fungus actually displays both transmission modes simultaneously, by choking some tillers and transmitting in seeds produced by unchoked tillers.

While beingobligate symbionts in nature, most epichloae are readily culturable in thelaboratory onculture media such aspotato dextrose agar or a minimal salts broth supplemented with thiamine, sugars or sugar alcohols, and organic nitrogen or ammonium.^[12]

Epichloë species are commonly spread byflies of the genusBotanophila. The flies lay their eggs in the growing fungal tissues and the larvae feed on them.^[13]

The epichloae display a number of central features that suggest a very strong and ancient association with their grass hosts. The symbiosis appears to have existed already during the early grassevolution that has spawned today'spooid grasses. This is suggested byphylogenetic studies indicating a preponderance of codivergence ofEpichloë species with the grass hosts they inhabit.^[14] Growth of the fungal symbiont is very tightly regulated within its grass host, indicated by a largely unbranchedmycelial morphology and remarkable synchrony of grass leaf andhyphal extension of the fungus;^[15][16] the latter seems to occur via a mechanism that involves stretch-induced orintercalary elongation of the endophyte's hyphae, a process so far not found in any other fungal species, indicating specialized adaptation of the fungus to the dynamic growth environment inside its host.^[17] A complexNADPH oxidase enzyme-basedROS-generating system inEpichloë species is indispensable for maintenance of this growth synchrony. Thus, it has been demonstrated thatdeletion of genes encoding these enzymes inEpichloë festucae causes severely disordered fungal growth in grass tissues and even death of the grass plant.^[18][19]

Molecular phylogenetic evidence demonstrates that asexualEpichloë species are derived either from sexualEpichloë species, or more commonly, are hybrids of two or more progenitorEpichloë species.^[20][21]

ManyEpichloë endophytes produce a diverse range ofnatural product compounds with biological activities against a broad range of herbivores.^[22][23] The purpose of these compounds is as atoxicity or feeding deterrence against insect and mammalianherbivores.^[24]Ergoline alkaloids (which are ergot alkaloids, named after theergot fungus,Claviceps purpurea, a close relative of the epichloae) are characterized by a ring system derived from 4-prenyltryptophan.^[25] Among the most abundant ergot alkaloids in epichloë-symbiotic grasses is ergovaline, comprising an ergolinemoiety attached to a bicyclictripeptide containing the amino acidsL-proline,L-alanine, andL-valine. Key genes and enzymes for ergot alkaloidbiosynthesis have been identified in epichloae and includedmaW, encodingdimethylallyl-tryptophan synthase andlpsA, anon-ribosomal peptide synthetase.^[25]

Another group of epichloë alkaloids are theindole-diterpenoids, such as lolitrem B, which are produced from the activity of several enzymes, includingprenyltransferases and variousmonooxygenases.^[26] Both the ergoline and indole-diterpenoid alkaloids havebiological activity against mammalian herbivores, and also activity against some insects.^[22]Peramine is a pyrrolopyrazine alkaloid thought to be biosynthesized from theguanidinium-group-containing amino acidL-arginine, and pyrrolidine-5-carboxylate, a precursor ofL-proline,^[27][28] and is an insect-feeding deterrent.^[28] One gene required for peramine synthesis –perA – was found by Tanakaet al., 2005.^[28] Theloline alkaloids^[29] are 1-aminopyrrolizidines with an oxygen atom linking bridgehead carbons 2 and 7, and are biosynthesized from the amino acidsL-proline andL-homoserine.^[30] The lolines haveinsecticidal and insect-deterrent activities comparable tonicotine.^[29] Loline accumulation is strongly induced in young growing tissues^[31] or by damage to the plant-fungus symbiotum.^[32] Many, but not all, epichloae produce up to three classes of these alkaloids in various combinations and amounts.^[22] Recently it has been shown thatEpichloë uncinata infection and loline content afford× Festulolium grasses protection from black beetle (Heteronychus arator).^[33]

Many species inEpichloë produce biologically active alkaloids, such asergot alkaloids, indole-diterpenoids (e.g.,lolitrem B),loline alkaloids, and the unusualguanidinium alkaloid, peramine.^[22]

It has been proposed that vertically transmittedsymbionts should evolve to bemutualists since their reproductivefitness is intimately tied to that of their hosts.^[34] In fact, some positive effects of epichloae on their host plants include increased growth, drought tolerance, andherbivore andpathogen resistance.^[10][35] Resistance against herbivores has been attributed toalkaloids produced by the symbiotic epichloae.^[22] Although grass-epichloë symbioses have been widely recognized to bemutualistic in many wild and cultivated grasses, the interactions can be highly variable and sometimes antagonistic, especially under nutrient-poor conditions in the soil.^[36]

Due to the relatively large number of grass species harboring epichloae and the variety of environments in which they occur, the mechanisms underlying beneficial or antagonistic outcomes of epichloë-grass symbioses are difficult to delineate in natural and also agricultural environments.^[10][37] Some studies suggest a relationship between grazing by herbivores and increased epichloë infestation of the grasses on which they feed,^[38][39] whereas others indicate a complex interplay between plant species and fungal symbionts in response to herbivory or environmental conditions.^[40] The strong anti-herbivore activities of several bioactive compounds produced by the epichloae^[22][27] and relatively modest direct effects of the epichloae on plant growth and physiology^[41][42] suggest that these compounds play a major role in the persistence of the symbiosis.

• Epichloë
• Hypocreales genera
• Taxa named by Elias Magnus Fries
• Taxa described in 1945

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