Epichole, also known as Epichloë, is a genus of ascomycete fungi forming an endophytic symbiosis with grasses. Grass choke disease is a symptom in grasses induced by some Epichloë species, which form spore-bearing mats (stromata) on tillers and suppress the development of their host plant's inflorescence. 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-deterring alkaloids, increased stress resistance, and growth promotion.
Within the family Clavicipitaceae, Epichloë is embedded in a group of endophytic and plant pathogenic fungi, whose common ancestor probably derived from an animal pathogen. The genus includes both species with a sexually reproducing (teleomorphic) stage and asexual, anamorphic species. The latter were previously placed in the form genus Neotyphodium but included in Epichloë after molecular phylogenetics had shown asexual and sexual species to be intermingled in a single clade. 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 of plant communities and food webs. Grass varieties, especially of tall fescue and ryegrass, with symbiotic Epichloë endophyte strains, are commercialised and used for pasture and turf.
Taxonomy
Elias Fries, in 1849, first defined Epichloë as a subgenus of Cordyceps. As type species, he designated Cordyceps typhina, originally described by Christiaan Hendrik Persoon. The brothers Charles and Louis René Tulasne then raised the subgenus to genus rank in 1865. 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. Several species from Africa and Asia that develop stromata on grasses were split off as a separate genus Parepichloe in 1998.
Many Epichloë species have forms that reproduce sexually, and several purely asexual species are closely related to them. These anamorphs were long classified separately: Morgan-Jones and Gams (1982) collected them in a section (Albo-lanosa) of genus Acremonium. In a molecular phylogenetic study in 1996, Glenn and colleagues found the genus to be polyphyletic and proposed a new genus Neotyphodium for the anamorphic species related to Epichloë. A number of species continued to be described in both genera until Leuchtmann and colleagues (2014) included most of the form genus Neotyphodium in Epichloë. Phylogenetic studies had shown both genera to be intermingled, and the nomenclatural code required since 2011 that one single name be used for all stages of development of a fungal species. Only Neotyphodium starrii, of unclear status, and N. chilense, which is unrelated, were excluded from Epichloë.
Species
As of 2024, there are 44 accepted species in the genus, with 1 subspecies and 5 varieties 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 in Neotyphodium.
Haploid Taxa Known Distribution Sexual Reproduction Vertical Transmission Known Host Range Reference to Species Description Epichloë amarillans J.F. White North America Observed Present Agrostis hyemalis, Agrostis perennans, Calamagrostis canadensis, Elymus virginicus, Sphenopholis nitida, Sphenopholis obtusata, Sphenopholis × pallens, Ammophila breviligulata Epichloë aotearoae (C.D. Moon, C.O. Miles & Schardl) Leuchtm. & Schardl New Zealand, Australia Not observed Present Echinopogon ovatus Epichloë baconii J.F. White Europe Observed Absent Agrostis capillaris, Agrostis stolonifera Epichloë brachyelytri Schardl & Leuchtm. North America Observed Present Brachyelytrum erectum Epichloë bromicola Leuchtm. & Schardl Europe, Asia Observed on Bromus erectus, Elymus repens and Elymus tsukushiensis Present in Bromus benekenii, Bromus ramosus, Bromus tomentellus, Elymus repens, Elymus tsukushiensis, Hordelymus europaeus, Hordeum brevisubulatum, Leymus chinensis, Melica persica Europe: Bromus benekenii, Bromus erectus, Bromus ramosus, Elymus repens, Hordelymus europaeus, Hordeum brevisubulatum. Asia: Bromus tomentellus, Leymus chinensis, Elymus tsukushiensis, Melica persica Epichloë calamagrostidis Leuchtm. & SchardlEuropeObserverdAbsentCalamagrostis villosa, Calamagrostis varia, Calamagrostis purpureaLeuchtmann, Adrian; Schardl, Christopher L. (2022). "Genetic diversity of Epichloë endophytes associated with Brachypodium and Calamagrostis host grass genera including two new species". Journal of Fungi. 8 (10): 1886. doi: 10.3390/jof8101086 Epichloë elymi Schardl & Leuchtm. North America Observed Present Bromus kalmii, Elymus spp. (including Elymus hystrix) Epichloë festucae Leuchtm., Schardl & M.R. Siegel Europe, Asia, North America Observed Present Festuca spp., Koeleria spp., Schedonorus spp. Epichloë festucae var. lolii (Latch, M.J. Chr. & Samuels) C.W. Bacon & Schardl Europe, Asia, North Africa, introduced in New Zealand, Australia and elsewhere Not observed Present Lolium perenne subsp. perenne Epichloë ftanensis Leuchtm. & A.D. TreindlEuropeObservedAbsentCalamagrostis arundinaceaLeuchtmann, Adrian; Schardl, Christopher L. (2022). "Genetic diversity of Epichloë endophytes associated with Brachypodium and Calamagrostis host grass genera including two new species". Journal of Fungi. 8 (10): 1886. doi: 10.3390/jof8101086 Epichloë gansuensis (C.J. Li & Nan) Schardl Asia Not observed Present Achnatherum inebrians, Achnatherum sibiricum, Achnatherum pekinense Epichloë inebrians (C.D. Moon & Schardl) L. Chen & C.J. Li Asia Not observed Present Achnatherum inebrians Epichloë glyceriae Schardl & Leuchtm. North America Observed Absent Glyceria spp. Epichloë mollis (Morgan-Jones & W. Gams) Leuchtm. & Schardl Europe Observed Present Holcus mollis Epichloë scottii T. Thünen, Y. Becker, M.P. Cox & S. Ashrafi Europe Observed Present Melica uniflora Epichloë sibirica (X. Zhang & Y.B. Gao) Tadych Asia Not observed Present Achnatherum sibiricum Epichloë stromatolonga (Y.L. Ji, L.H. Zhan & Z.W. Wang) Leuchtm. Asia Not observed Present Calamagrostis epigejos Epichloë sylvatica Leuchtm. & Schardl Europe, Asia Observed Present Brachypodium sylvaticum, Hordelymus europaeus Epichloë sylvatica subsp. pollinensis Leuchtm. & M. Oberhofer Europe Observed Present Hordelymus europaeus Epichloë typhina (Pers.) Brockm. Europe, introduced in North America and elsewhere Observed Present in Puccinellia distans; absent in other hosts Anthoxanthum odoratum, Brachypodium phoenicoides, Brachypodium pinnatum, Dactylis glomerata, Lolium perenne, Milium effusum, Phleum pratense, Poa trivialis, Poa silvicola, Puccinellia distans Epichloë clarkii J.F. White Europe Observed Absent Holcus lanatus Holcus mollis Epichloë poae Tadych, K.V. Ambrose, F.C. Belanger & J.F. White Europe, North America Observed on Poa nemoralis and Poa pratensis Present in Poa nemoralis, Poa secunda subsp. juncifolia; absent in Poa pratensis Europe: Poa nemoralis, Poa pratensis. North America: Poa secunda subsp. juncifolia, Poa sylvestris Epichloë poae var. aonikenkana Iannone & Schardl Argentina (Santa Cruz) Not observed Present Bromus setifolius Epichloë poae var. canariensis (C.D. Moon, B. Scott, & M.J. Chr.) Leuchtm. Canary Islands Not observed Present Lolium edwardii Epichloë poae var. huerfana (J.F. White, G.T. Cole & Morgan-Jones) Tadych & Leuchtm. North America Not observed Present Festuca arizonica
Hybrid Taxa Progenitor Species Known Distribution Sexual Reproduction Vertical Transmission Known Host Range Reference to Species Description Epichloë alsodes T. Shymanovich, C.A. Young, N.D. Charlton & S.H. Faeth Epichloë amarillans × Epichloë typhina subsp. poae North America Not observed Present Poa alsodes Epichloë australiensis (C.D. Moon & Schardl) Leuchtm. & Schardl Epichloë festucae × Epichloë typhina complex (from Poa pratensis) Australia Not observed Present Echinopogon ovatus Epichloë cabralii Iannone, M.S. Rossi & Schardl Epichloë amarillans × Epichloë typhina complex (from Poa nemoralis) Argentina (Santa Cruz, Tierra del Fuego) Not observed Present Phleum alpinum Epichloë canadensis N.D. Charlton & C.A. Young Epichloë amarillans × Epichloë elymi North America Not observed Present Elymus canadensis Epichloë chisosa (J.F. White & Morgan-Jones) Schardl Epichloë amarillans × Epichloë bromicola × Epichloë typhina complex (from Poa pratensis) North America Not observed Present Achnatherum eminens Epichloë coenophiala (Morgan-Jones & W. Gams) C.W. Bacon & Schardl Epichloë baconii (Lolium associated clade) × Epichloë festucae × Epichloë typhina complex (from Poa nemoralis) Europe, North Africa, introduced in North America and elsewhere Not observed Present Schedonorus arundinaceus [synonyms: Festuca arundinacea, Lolium arundinaceum] Epichloë danica Leuchtm. & M. Oberhofer Epichloë bromicola × Epichloë sylvatica Europe Not observed Present Hordelymus europaeus Epichloë disjuncta Leuchtm. & M. Oberhofer Epichloë scottii × Epichloë typhina complex Europe Not observed Present Hordelymus europaeus Epichloë funkii (K.D. Craven & Schardl) J.F. White Epichloë elymi × Epichloë festucae North America Not observed Present Achnatherum robustum Epichloë guerinii (Guillaumin, Ravel & C.D. Moon) Leuchtm. & Schardl Epichloë gansuensis × Epichloë typhina complex Europe Not observed Present Melica ciliata, Melica transsilvanica Epichloë hordelymi Leuchtm. & M. Oberhofer Epichloë bromicola × Epichloë typhina complex Europe Not observed Present Hordelymus europaeus Epichloë hybrida M.P. Cox & M.A. Campbell Epichloë festucae var. lolii × Epichloë typhina Europe Not observed Present Lolium perenne Epichloë liyangensis Z.W. Wang, Y. Kang & H. Miao Epichloë bromicola × Epichloë typhina complex (from Poa nemoralis) Asia Observed Present Poa pratensis subsp. pratensis Epichloë melicicola (C.D. Moon & Schardl) Schardl Epichloë aotearoae × Epichloë festucae South Africa Not observed Present Melica racemosa, Melica decumbens Epichloë novae-zelandiae Leuchtm. & A.V. Stewart Epichloë amarillans × Epichloë bromicola × Epichloë typhina subsp. poae New Zealand Not observed Present Poa matthewsii Epichloë occultans (C.D. Moon, B. Scott & M.J. Chr.) Schardl Epichloë baconii (Lolium associated clade) × Epichloë bromicola Europe, North Africa, introduced in New Zealand and elsewhere Not observed Present Lolium multiflorum, Lolium rigidum u.a. Epichloë pampeana (Iannone & Cabral) Iannone & Schardl Epichloë festucae × Epichloë typhina complex (from Poa nemoralis) South America Not observed Present Bromus auleticus Epichloë schardlii (Ghimire, Rudgers & K.D. Craven) Leuchtm. Epichloë typhina complex (subsp. poae × subsp. poae) North America Not observed Present Cinna arundinacea Epichloë schardlii var. pennsylvanica T. Shymanovich, C.A. Young, N.D. Charlton & S.H. Faeth Epichloë typhina complex (subsp. poae × subsp. poae) North America Not observed Present Poa alsodes Epichloë siegelii (K.D. Craven, Leuchtm. & Schardl) Leuchtm. & Schardl Epichloë bromicola × Epichloë festucae Europe Not observed Present Schedonorus pratensis (synonyms: Festuca pratensis, Lolium pratense) Epichloë sinensis P. Tian, C.J. Li & Z.B. Nan Epichloë sibirica × Epichloë typhina subsp. poae Asia (Northwest China) Not observed Present Festuca sinensis Epichloë sinica (Z.W. Wang, Y.L. Ji & Y. Kang) Leuchtm. Epichloë bromicola × Epichloë typhina complex Asia Not observed Present Roegneria spp. Epichloë sinofestucae