Epichloë

Epichloë
"Choke disease": Epichloë typhina stroma on bluegrass
Scientific classification Edit this classification
Domain: Eukaryota
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. Epichloë Fr. (1849)
  • Hyperdermium J.F.White (2000)
  • Neotyphodium Glenn (1996)

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

[edit]

Elias Fries, in 1849, first defined Epichloë as a subgenus of Cordyceps.[2] As type species, he designated Cordyceps typhina,[2] originally described by Christiaan Hendrik Persoon.[3] The brothers Charles and Louis 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 genus Parepichloe in 1998.[6]

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.[7] 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.[8] 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.[5] 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.[5]

Phylogeny of the fungal genus Epichloë from aligned tubB gene sequences.Epichloë amarillansEpichloë aotearoaeEpichloë baconiiEpichloë brachyelytriEpichloë bromicolaEpichloë elymiEpichloë festucaeEpichloë gansuensisEpichloë glyceriaeEpichloë mollisEpichloë sibiricaEpichloë stromatolongaEpichloë sylvaticaEpichloë typhinaEpichloë typhina
Phylogeny of the genus *Epichloë*. Clicking on a species in the phylogeny will load the appropriate wikipedia article.

Species

[edit]

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.[5]

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 White, James F. (1994). "Endophyte-host associations in grasses. XX. Structural and reproductive studies of Epichloë amarillans sp. nov. and comparisons to E. typhina". Mycologia. 86 (4): 571–580. doi:10.1080/00275514.1994.12026452. ISSN 0027-5514.
Epichloë aotearoae

(C.D. Moon, C.O. Miles & Schardl) Leuchtm. & Schardl

New Zealand, Australia Not observed Present Echinopogon ovatus Moon, Christina D.; Miles, Christopher O.; Järlfors, Ulla; Schardl, Christopher L. (2002). "The evolutionary origins of three new Neotyphodium endophyte species from grasses indigenous to the Southern Hemisphere". Mycologia. 94 (4): 694–711. doi:10.1080/15572536.2003.11833197. ISSN 0027-5514. PMID 21156542. S2CID 12259278.
Epichloë baconii

J.F. White

Europe Observed Absent Agrostis capillaris, Agrostis stolonifera White, James F. (1993). "Endophyte-host associations in grasses. XIX. A systematic study of some sympatric species of Epichloë in England". Mycologia. 85 (3): 444–455. doi:10.1080/00275514.1993.12026295. ISSN 0027-5514.
Epichloë brachyelytri

Schardl & Leuchtm.

North America Observed Present Brachyelytrum erectum Schardl, Christopher L.; Leuchtmann, Adrian (1999). "Three new species of Epichloë symbiotic with North American grasses". Mycologia. 91 (1): 95–107. doi:10.1080/00275514.1999.12060996. ISSN 0027-5514.
Epichloë bromicola

Leuchtm. & Schardl

Europe, Asia Observed on Bromus erectus, Elymus repens and Elymus tsukushiensis Present in Bromus benekenii, Bromus ramosus and Hordelymus europaeus, Hordeum brevisubulatum, Leymus chinensis and Elymus tsukushiensis; absent in Bromus erectus and Elymus repens Europe: Bromus benekenii, Bromus erectus, Bromus ramosus, Elymus repens, Hordelymus europaeus, Hordeum brevisubulatum. Asia: Leymus chinensis, Elymus tsukushiensis Leuchtmann, Adrian; Schardl, Christopher L. (1998). "Mating compatibility and phylogenetic relationships among two new species of Epichloë and other congeneric European species". Mycological Research. 102 (10): 1169–1182. doi:10.1017/S0953756298006236. ISSN 0953-7562.
Epichloë calamagrostidis

Leuchtm. & Schardl

Europe Observerd Absent Calamagrostis villosa, Calamagrostis varia, Calamagrostis purpurea Leuchtmann, 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) Schardl, Christopher L.; Leuchtmann, Adrian (1999). "Three new species of Epichloë symbiotic with North American grasses". Mycologia. 91 (1): 95–107. doi:10.1080/00275514.1999.12060996. ISSN 0027-5514.
Epichloë festucae

Leuchtm., Schardl & M.R. Siegel

Europe, Asia, North America Observed Present Festuca spp., Koeleria spp., Schedonorus spp. Leuchtmann, Adrian; Schardl, Christopher L.; Siegel, Malcolm R. (1994). "Sexual compatibility and taxonomy of a new species of Epichloë symbiotic with fine fescue grasses". Mycologia. 86 (6): 802–812. doi:10.1080/00275514.1994.12026487. ISSN 0027-5514.
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 Latch, G.C.M.; Christensen, M.J.; Samuels, G.J. (1984). "Five endophytes of Lolium and Festuca in New Zealand". Mycotaxon. 20: 535–550.
Epichloë ftanensis Leuchtm. & A.D. Treindl Europe Observed Absent Calamagrostis arundinacea Leuchtmann, 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 Li, C.J.; Nan, Z.B.; Paul, V.H.; Dapprich, P.D.; Liu, Y. (2004). "A new Neotyphodium species symbiotic with drunken horse grass (Achnatherum inebrians) in China". Mycotaxon. 90: 141–147.
Epichloë inebrians

(C.D. Moon & Schardl) L. Chen & C.J. Li

Asia Not observed Present Achnatherum inebrians Moon, Christina D.; Guillaumin, Jean-Jacques; Ravel, Catherine; Li, Chunjie; Craven, Kelly D.; Schardl, Christopher L. (2007). "New Neotyphodium endophyte species from the grass tribes Stipeae and Meliceae". Mycologia. 99 (6): 895–905. doi:10.1080/15572536.2007.11832521. ISSN 0027-5514. PMID 18333513. S2CID 19953493.
Epichloë glyceriae

Schardl & Leuchtm.

North America Observed Absent Glyceria spp. Schardl, Christopher L.; Leuchtmann, Adrian (1999). "Three new species of Epichloë symbiotic with North American grasses". Mycologia. 91 (1): 95–107. doi:10.1080/00275514.1999.12060996. ISSN 0027-5514.
Epichloë mollis

(Morgan-Jones & W. Gams) Leuchtm. & Schardl

Europe Observed Present Holcus mollis Morgan-Jones, G.; Gams, W. (1982). "Notes on hyphomycetes. XLI. An endophyte of Festuca arundinacea and the anamorph of Epichloë typhina, new taxa in one of two new sections of Acremonium". Mycotaxon. 15: 311–318. ISSN 0093-4666.
Epichloë scottii

T. Thünen, Y. Becker, M.P. Cox & S. Ashrafi

Europe Observed Present Melica uniflora Thünen, Torsten; Becker, Yvonne; Cox, Murray P.; Ashrafi, Samad (2022). "Epichloë scottii sp. nov., a new endophyte isolated from Melica uniflora is the missing ancestor of Epichloë disjuncta". IMA Fungus. 13 (1): 2. doi:10.1186/s43008-022-00088-0. PMC 8812020. PMID 35109929.
Epichloë sibirica

(X. Zhang & Y.B. Gao) Tadych

Asia Not observed Present Achnatherum sibiricum Zhang, Xin; Ren, An-Zhi; Wei, Yu-Kun; Lin, Feng; Li, Chuan; Liu, Zhi-Jian; Gao, Yu-Bao (2009). "Taxonomy, diversity and origins of symbiotic endophytes of Achnatherum sibiricum in the Inner Mongolia Steppe of China". FEMS Microbiology Letters. 301 (1): 12–20. doi:10.1111/j.1574-6968.2009.01789.x. ISSN 0378-1097. PMID 19863662.
Epichloë stromatolonga

(Y.L. Ji, L.H. Zhan & Z.W. Wang) Leuchtm.

Asia Not observed Present Calamagrostis epigejos Ji, Yan-ling; Zhan, Li-hui; Kang, Yan; Sun, Xiang-hui; Yu, Han-shou; Wang, Zhi-wei (2009). "A new stromata-producing Neotyphodium species symbiotic with clonal grass Calamagrostis epigeios (L.) Roth. grown in China". Mycologia. 101 (2): 200–205. doi:10.3852/08-044. ISSN 0027-5514. PMID 19397192. S2CID 32237846.
Epichloë sylvatica

Leuchtm. & Schardl

Europe, Asia Observed Present Brachypodium sylvaticum, Hordelymus europaeus Leuchtmann, Adrian; Schardl, Christopher L. (1998). "Mating compatibility and phylogenetic relationships among two new species of Epichloë and other congeneric European species". Mycological Research. 102 (10): 1169–1182. doi:10.1017/S0953756298006236. ISSN 0953-7562.
Epichloë sylvatica subsp. pollinensis

Leuchtm. & M. Oberhofer

Europe Observed Present Hordelymus europaeus Leuchtmann, Adrian; Oberhofer, Martina (2013). "The Epichloë endophytes associated with the woodland grass Hordelymus europaeus including four new taxa". Mycologia. 105 (5): 1315–1324. doi:10.3852/12-400. ISSN 0027-5514. PMID 23921239. S2CID 21024362.
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 Brockmüller, H. J. H (1863). "Beiträge zur Kryptogamen-Flora Mecklenburgs". Archiv der Freunde der Naturgeschichte in Mecklenburg. 17: 162–256.
Epichloë clarkii

J.F. White

Europe Observed Absent Holcus lanatus

Holcus mollis

White, James F. (1993). "Endophyte-host associations in grasses. XIX. A systematic study of some sympatric species of Epichloë in England". Mycologia. 85 (3): 444–455. doi:10.1080/00275514.1993.12026295. ISSN 0027-5514.
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 Tadych, Mariusz; Ambrose, Karen V.; Bergen, Marshall S.; Belanger, Faith C.; White, James F. (2012). "Taxonomic placement of Epichloë poae sp. nov. and horizontal dissemination to seedlings via conidia". Fungal Diversity. 54 (1): 117–131. doi:10.1007/s13225-012-0170-0. ISSN 1560-2745. S2CID 17813728.
Epichloë poae var. aonikenkana

Iannone & Schardl

Argentina (Santa Cruz) Not observed Present Bromus setifolius Mc Cargo, Patricia D.; Iannone, Leopoldo J.; Vignale, María Victoria; Schardl, Christopher L.; Rossi, María Susana (2017). "Species diversity of Epichloë symbiotic with two grasses from southern Argentinean Patagonia". Mycologia. 106 (2): 339–352. doi:10.3852/106.2.339. hdl:11336/37491. ISSN 0027-5514. PMID 24782501. S2CID 44547876.
Epichloë poae var. canariensis

(C.D. Moon, B. Scott, & M.J. Chr.) Leuchtm.

Canary Islands Not observed Present Lolium edwardii Moon, Christina D.; Scott, Barry; Schardl, Christopher L.; Christensen, Michael J. (2000). "The evolutionary origins of Epichloë endophytes from annual ryegrasses". Mycologia. 92 (6): 1103–1118. doi:10.1080/00275514.2000.12061258. ISSN 0027-5514. S2CID 218589443.
Epichloë poae var. huerfana

(J.F. White, G.T. Cole & Morgan-Jones) Tadych & Leuchtm.

North America Not observed Present Festuca arizonica Glenn, Anthony E.; Bacon, Charles W.; Price, Robert; Hanlin, Richard T. (1996). "Molecular phylogeny of Acremonium and its taxonomic implications". Mycologia. 88 (3): 369–383. doi:10.1080/00275514.1996.12026664. ISSN 0027-5514.
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 Shymanovich, Tatsiana; Charlton, Nikki D.; Musso, Ashleigh M.; Scheerer, Jonathan; Cech, Nadja B.; Faeth, Stanley H.; Young, Carolyn A. (2017). "Interspecific and intraspecific hybrid Epichloë species symbiotic with the North American native grass Poa alsodes" (PDF). Mycologia. 109 (3): 459–474. doi:10.1080/00275514.2017.1340779. ISSN 0027-5514. PMID 28723242. S2CID 25290203.
Epichloë australiensis

(C.D. Moon & Schardl) Leuchtm. & Schardl

Epichloë festucae × Epichloë typhina complex (from Poa pratensis) Australia Not observed Present Echinopogon ovatus Moon, Christina D.; Miles, Christopher O.; Järlfors, Ulla; Schardl, Christopher L. (2017). "The evolutionary origins of three new Neotyphodium endophyte species from grasses indigenous to the Southern Hemisphere". Mycologia. 94 (4): 694–711. doi:10.1080/15572536.2003.11833197. ISSN 0027-5514. PMID 21156542. S2CID 12259278.
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 Mc Cargo, Patricia D.; Iannone, Leopoldo J.; Vignale, María Victoria; Schardl, Christopher L.; Rossi, María Susana (2017). "Species diversity of Epichloë symbiotic with two grasses from southern Argentinean Patagonia". Mycologia. 106 (2): 339–352. doi:10.3852/106.2.339. hdl:11336/37491. ISSN 0027-5514. PMID 24782501. S2CID 44547876.
Epichloë canadensis

N.D. Charlton & C.A. Young

Epichloë amarillans × Epichloë elymi North America Not observed Present Elymus canadensis Charlton, N. D.; Craven, K. D.; Mittal, S.; Hopkins, A. A.; Young, C. A. (2012). "Epichloë canadensis, a new interspecific epichloid hybrid symbiotic with Canada wildrye (Elymus canadensis)". Mycologia. 104 (5): 1187–1199. doi:10.3852/11-403. ISSN 0027-5514. PMID 22675049. S2CID 43674700.
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 Glenn, Anthony E.; Bacon, Charles W.; Price, Robert; Hanlin, Richard T. (2018). "Molecular phylogeny of Acremonium and its taxonomic implications". Mycologia. 88 (3): 369–383. doi:10.1080/00275514.1996.12026664. ISSN 0027-5514.
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] Morgan-Jones, G.; Gams, W. (1982). "Notes on hyphomycetes. XLI. An endophyte of Festuca arundinacea and the anamorph of Epichloë typhina, new taxa in one of two new sections of Acremonium". Mycotaxon. 15: 311–318. ISSN 0093-4666.
Epichloë danica

Leuchtm. & M. Oberhofer

Epichloë bromicola × Epichloë sylvatica Europe Not observed Present Hordelymus europaeus Leuchtmann, Adrian; Oberhofer, Martina (2017). "The Epichloë endophytes associated with the woodland grass Hordelymus europaeus including four new taxa". Mycologia. 105 (5): 1315–1324. doi:10.3852/12-400. ISSN 0027-5514. PMID 23921239. S2CID 21024362.
Epichloë disjuncta

Leuchtm. & M. Oberhofer

Epichloë scottii × Epichloë typhina complex Europe Not observed Present Hordelymus europaeus Leuchtmann, Adrian; Oberhofer, Martina (2017). "The Epichloë endophytes associated with the woodland grass Hordelymus europaeus including four new taxa". Mycologia. 105 (5): 1315–1324. doi:10.3852/12-400. ISSN 0027-5514. PMID 23921239. S2CID 21024362.
Epichloë funkii

(K.D. Craven & Schardl) J.F. White

Epichloë elymi × Epichloë festucae North America Not observed Present Achnatherum robustum Moon, Christina D.; Guillaumin, Jean-Jacques; Ravel, Catherine; Li, Chunjie; Craven, Kelly D.; Schardl, Christopher L. (2017). "New Neotyphodium endophyte species from the grass tribes Stipeae and Meliceae". Mycologia. 99 (6): 895–905. doi:10.1080/15572536.2007.11832521. ISSN 0027-5514. PMID 18333513. S2CID 19953493.
Epichloë guerinii

(Guillaumin, Ravel & C.D. Moon) Leuchtm. & Schardl

Epichloë gansuensis × Epichloë typhina complex Europe Not observed Present Melica ciliata, Melica transsilvanica Moon, Christina D.; Guillaumin, Jean-Jacques; Ravel, Catherine; Li, Chunjie; Craven, Kelly D.; Schardl, Christopher L. (2017). "New Neotyphodium endophyte species from the grass tribes Stipeae and Meliceae". Mycologia. 99 (6): 895–905. doi:10.1080/15572536.2007.11832521. ISSN 0027-5514. PMID 18333513. S2CID 19953493.
Epichloë hordelymi

Leuchtm. & M. Oberhofer

Epichloë bromicola × Epichloë typhina complex Europe Not observed Present Hordelymus europaeus Leuchtmann, Adrian; Oberhofer, Martina (2017). "The Epichloë endophytes associated with the woodland grass Hordelymus europaeus including four new taxa". Mycologia. 105 (5): 1315–1324. doi:10.3852/12-400. ISSN 0027-5514. PMID 23921239. S2CID 21024362.
Epichloë hybrida

M.P. Cox & M.A. Campbell

Epichloë festucae var. lolii × Epichloë typhina Europe Not observed Present Lolium perenne Campbell, Matthew A.; Tapper, Brian A.; Simpson, Wayne R.; Johnson, Richard D.; Mace, Wade; Ram, Arvina; Lukito, Yonathan; Dupont, Pierre-Yves; Johnson, Linda J.; Scott, D. Barry; Ganley, Austen R. D.; Cox, Murray P. (2017). "Epichloë hybrida, sp. nov., an emerging model system for investigating fungal allopolyploidy". Mycologia. 109 (5): 1–15. doi:10.1080/00275514.2017.1406174. ISSN 0027-5514. PMID 29370579.
Epichloë liyangensis

Z.W. Wang, Y. Kang & H. Miao

Epichloë bromicola × Epichloë typhina complex (from Poa nemoralis) Asia Observed Present Poa pratensis subsp. pratensis Yan, Kang; Yanling, Ji; Kunran, Zhu; Hui, Wang; Huimin, Miao; Zhiwei, Wang (2017). "A new Epichloë species with interspecific hybrid origins from Poa pratensis ssp. pratensis in Liyang, China". Mycologia. 103 (6): 1341–1350. doi:10.3852/10-352. ISSN 0027-5514. PMID 21659456. S2CID 22672333.
Epichloë melicicola

(C.D. Moon & Schardl) Schardl

Epichloë aotearoae × Epichloë festucae South Africa Not observed Present Melica racemosa, Melica decumbens Moon, Christina D.; Miles, Christopher O.; Järlfors, Ulla; Schardl, Christopher L. (2017). "The evolutionary origins of three new Neotyphodium endophyte species from grasses indigenous to the Southern Hemisphere". Mycologia. 94 (4): 694–711. doi:10.1080/15572536.2003.11833197. ISSN 0027-5514. PMID 21156542. S2CID 12259278.
Epichloë novae-zelandiae

Leuchtm. & A.V. Stewart

Epichloë amarillans × Epichloë bromicola × Epichloë typhina subsp. poae New Zealand Not observed Present Poa matthewsii Leuchtmann, Adrian; Young, Carolyn A.; Stewart, Alan V.; Simpson, Wayne R.; Hume, David E.; Scott, Barry (2019). "Epichloë novae-zelandiae, a new endophyte from the endemic New Zealand grass Poa matthewsii". New Zealand Journal of Botany. 57 (4): 271–288. Bibcode:2019NZJB...57..271L. doi:10.1080/0028825X.2019.1651344. ISSN 0028-825X. S2CID 202012350.
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. Moon, Christina D.; Scott, Barry; Schardl, Christopher L.; Christensen, Michael J. (2019). "The evolutionary origins of Epichloë endophytes from annual ryegrasses". Mycologia. 92 (6): 1103–1118. doi:10.1080/00275514.2000.12061258. ISSN 0027-5514. S2CID 218589443.
Epichloë pampeana

(Iannone & Cabral) Iannone & Schardl

Epichloë festucae × Epichloë typhina complex (from Poa nemoralis) South America Not observed Present Bromus auleticus Iannone, Leopoldo Javier; Cabral, Daniel; Schardl, Christopher Lewis; Rossi, María Susana (2017). "Phylogenetic divergence, morphological and physiological differences distinguish a new Neotyphodium endophyte species in the grass Bromus auleticus from South America". Mycologia. 101 (3): 340–351. doi:10.3852/08-156. ISSN 0027-5514. PMID 19537207. S2CID 24799520.
Epichloë schardlii

(Ghimire, Rudgers & K.D. Craven) Leuchtm.

Epichloë typhina complex (subsp. poae × subsp. poae) North America Not observed Present Cinna arundinacea Ghimire, Sita R.; Rudgers, Jennifer A.; Charlton, Nikki D.; Young, Carolyn; Craven, Kelly D. (2017). "Prevalence of an intraspecific Neotyphodium hybrid in natural populations of stout wood reed (Cinna arundinacea L.) from eastern North America". Mycologia. 103 (1): 75–84. doi:10.3852/10-154. ISSN 0027-5514. PMID 20943524. S2CID 13556418.
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 Shymanovich, Tatsiana; Charlton, Nikki D.; Musso, Ashleigh M.; Scheerer, Jonathan; Cech, Nadja B.; Faeth, Stanley H.; Young, Carolyn A. (2017). "Interspecific and intraspecific hybrid Epichloë species symbiotic with the North American native grass Poa alsodes" (PDF). Mycologia. 109 (3): 459–474. doi:10.1080/00275514.2017.1340779. ISSN 0027-5514. PMID 28723242. S2CID 25290203.
Epichloë siegelii

(K.D. Craven, Leuchtm. & Schardl) Leuchtm. & Schardl

Epichloë bromicola × Epichloë festucae Europe Not observed Present Schedonorus pratensis (synonyms: Festuca pratensis, Lolium pratense) Craven, K.D.; Blankenship, J.D.; Leuchtmann, A.; Hinight, K.; Schardl, C.L. (2001). "Hybrid fungal endophytes symbiotic with the grass Lolium pratense". Sydowia. 53: 44–73.
Epichloë sinensis

P. Tian, C.J. Li & Z.B. Nan

Epichloë sibirica × Epichloë typhina subsp. poae Asia (Northwest China) Not observed Present Festuca sinensis Tian, Pei; Xu, Wenbo; Li, Chunjie; Song, Hui; Wang, Meining; Schardl, Christopher L.; Nan, Zhibiao (2020). "Phylogenetic relationship and taxonomy of a hybrid Epichloë species symbiotic with Festuca sinensis". Mycological Progress. 19 (10): 1069–1081. Bibcode:2020MycPr..19.1069T. doi:10.1007/s11557-020-01618-z. S2CID 225161777.
Epichloë sinica

(Z.W. Wang, Y.L. Ji & Y. Kang) Leuchtm.

Epichloë bromicola × Epichloë typhina complex Asia Not observed Present Roegneria spp. Yan, Kang; Yanling, Ji; Xianghui, Sun; Lihui, Zhan; Wei, Li; Hanshou, Yu; Zhiwei, Wang (2017). "Taxonomy of Neotyphodium endophytes of Chinese native Roegneria plants". Mycologia. 101 (2): 211–219. doi:10.3852/08-018. ISSN 0027-5514. PMID 19397194. S2CID 6307330.
Epichloë sinofestucae

(Y.G. Chen, Y.L. Ji & Z.W. Wang) Leuchtm.

Epichloë bromicola × Epichloë typhina complex Asia Not observed Present Festuca parvigluma Chen, Yong-gan; Ji, Yan-ling; Yu, Han-shou; Wang, Zhi-wei (2017). "A new Neotyphodium species from Festuca parvigluma Steud. grown in China". Mycologia. 101 (5): 681–685. doi:10.3852/08-181. ISSN 0027-5514. PMID 19750947. S2CID 27915317.
Epichloë tembladerae

(Cabral & J.F. White) Iannone & Schardl

Epichloë festucae × Epichloë typhina complex (from Poa nemoralis) North America Not observed Present North America: Festuca arizonica. South America: Bromus auleticus, Bromus setifolius, Festuca argentina, Festuca hieronymi, Festuca magellanica, Festuca superba, Melica stuckertii, Phleum alpinum, Phleum commutatum, Poa huecu, Poa rigidifolia Cabral, Daniel; Cafaro, Matías J.; Saidman, B.; Lugo, M.; Reddy, Ponaka V.; White, James F. (2019). "Evidence supporting the occurrence of a new species of endophyte in some South American grasses". Mycologia. 91 (2): 315–325. doi:10.1080/00275514.1999.12061021. ISSN 0027-5514.
Epichloë uncinata

(W. Gams, Petrini & D. Schmidt) Leuchtm. & Schardl

Epichloë bromicola × Epichloë typhina complex Europe Not observed Present Schedonorus pratensis (synonyms: Festuca pratensis, Lolium pratense) Gams, W.; Petrini, O. J.; Schmidt, D. (1990). "Acremonium uncinatum, a new endophyte in Festuca pratensis". Mycotaxon. 37: 67–71.A1:G25

Life cycle and growth

[edit]
Blue-stained large plant cells with smaller hyphae visible between them
Epichloë coenophiala hyphae between tall fescue leaf cells

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 the grasses and sedges, 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 host tiller, 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 thereby transmitted vertically to the next host generation. Most Epichloë species, and all asexual species, can vertically transmit.

The taxonomic dichotomy is especially interesting in this group of symbionts, because vegetative propagation of fungal mycelium occurs by vertical transmission, i.e., fungal growth into newly developing host tillers (=individual grass plants). Importantly, many Epichloë 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 in Epichloë species — causes "choke disease", a condition in which grass inflorescences 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 being obligate symbionts in nature, most epichloae are readily culturable in the laboratory on culture media such as potato 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 by flies of the genus Botanophila. The flies lay their eggs in the growing fungal tissues and the larvae feed on them.[13]

A stroma of Epichloë baconii formed on the grass Agrostis stolonifera, showing eggs, brood chambers and larval feeding tracks of Botanophila flies.

Evolution

[edit]

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 grass evolution that has spawned today's pooid grasses. This is suggested by phylogenetic studies indicating a preponderance of codivergence of Epichloë 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 unbranched mycelial morphology and remarkable synchrony of grass leaf and hyphal extension of the fungus;[15][16] the latter seems to occur via a mechanism that involves stretch-induced or intercalary 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 complex NADPH oxidase enzyme-based ROS-generating system in Epichloë species is indispensable for maintenance of this growth synchrony. Thus, it has been demonstrated that deletion of genes encoding these enzymes in Epichloë festucae causes severely disordered fungal growth in grass tissues and even death of the grass plant.[18][19]

Molecular phylogenetic evidence demonstrates that asexual Epichloë species are derived either from sexual Epichloë species, or more commonly, are hybrids of two or more progenitor Epichloë species.[20][21]

Bioactive compounds

[edit]
N-formylloline, an insecticidal alkaloid produced in several Epichloë–grass symbiota.

Many Epichloë endophytes produce a diverse range of natural product compounds with biological activities against a broad range of herbivores.[22][23] The purpose of these compounds is as a toxicity or feeding deterrence against insect and mammalian herbivores.[24] Ergoline alkaloids (which are ergot alkaloids, named after the ergot fungus, Claviceps purpurea, a close relative of the epichloae) are characterized by a ring system derived from 4-prenyl tryptophan.[25] Among the most abundant ergot alkaloids in epichloë-symbiotic grasses is ergovaline, comprising an ergoline moiety attached to a bicyclic tripeptide containing the amino acids L-proline, L-alanine, and L-valine. Key genes and enzymes for ergot alkaloid biosynthesis have been identified in epichloae and include dmaW, encoding dimethylallyl-tryptophan synthase and lpsA, a non-ribosomal peptide synthetase.[25]

Another group of epichloë alkaloids are the indole-diterpenoids, such as lolitrem B, which are produced from the activity of several enzymes, including prenyltransferases and various monooxygenases.[26] Both the ergoline and indole-diterpenoid alkaloids have biological activity against mammalian herbivores, and also activity against some insects.[22] Peramine is a pyrrolopyrazine alkaloid thought to be biosynthesized from the guanidinium-group-containing amino acid L-arginine, and pyrrolidine-5-carboxylate, a precursor of L-proline,[27][28] and is an insect-feeding deterrent.[28] One gene required for peramine synthesis – perA – was found by Tanaka et al., 2005.[28] The loline alkaloids[29] are 1-aminopyrrolizidines with an oxygen atom linking bridgehead carbons 2 and 7, and are biosynthesized from the amino acids L-proline and L-homoserine.[30] The lolines have insecticidal and insect-deterrent activities comparable to nicotine.[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 that Epichloë uncinata infection and loline content afford × Festulolium grasses protection from black beetle (Heteronychus arator).[33]

Many species in Epichloë produce biologically active alkaloids, such as ergot alkaloids, indole-diterpenoids (e.g., lolitrem B), loline alkaloids, and the unusual guanidinium alkaloid, peramine.[22]

Ecology

[edit]

Effects on the grass plant

[edit]

It has been proposed that vertically transmitted symbionts should evolve to be mutualists since their reproductive fitness 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, and herbivore and pathogen resistance.[10][35] Resistance against herbivores has been attributed to alkaloids produced by the symbiotic epichloae.[22] Although grass-epichloë symbioses have been widely recognized to be mutualistic in many wild and cultivated grasses, the interactions can be highly variable and sometimes antagonistic, especially under nutrient-poor conditions in the soil.[36]

Ecosystem dynamics

[edit]

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.

References

[edit]
  1. ^ "Synonymy: Epichloe (Fr.) Tul. & C. Tul. [as 'Epichloë'], Select. fung. carpol. (Paris) 3: 24 (1865)". Species Fungorum. Retrieved 1 August 2021.
  2. ^ a b Fries, E.M. (1849). Summa vegetabilium Scandinaviae (in Latin). Stockholm, Leipzig: Bonnier. p. 572.
  3. ^ Persoon, C.H. (1798). Icones et Descriptiones Fungorum Minus Cognitorum (in Latin). Leipzig: Bibliopolii Breitkopf-Haerteliani impensis. Open access icon
  4. ^ Tulasne, L.R.; Tulasne, C. (1865). Selecta Fungorum Carpologia: Nectriei – Phacidiei – Pezizei (in Latin). Vol. 3.
  5. ^ a b c d Leuchtmann, A.; Bacon, C. W.; Schardl, C. L.; White, J. F.; Tadych, M. (2014). "Nomenclatural realignment of Neotyphodium species with genus Epichloë" (PDF). Mycologia. 106 (2): 202–215. doi:10.3852/13-251. ISSN 0027-5514. PMID 24459125. S2CID 25222557. Archived from the original (PDF) on 2016-03-07. Retrieved 2016-02-28.
  6. ^ White, J.F.; Reddy, P.V. (1998). "Examination of Structure and Molecular Phylogenetic Relationships of Some Graminicolous Symbionts in Genera Epichloe and Parepichloe". Mycologia. 90 (2): 226. doi:10.2307/3761298. ISSN 0027-5514. JSTOR 3761298.
  7. ^ Morgan-Jones, G.; Gams, W. (1982). "Notes on hyphomycetes. XLI. An endophyte of Festuca arundinacea and the anamorph of Epichloe typhina, new taxa in one of two new sections of Acremonium". Mycotaxon. 15: 311–318. ISSN 0093-4666.
  8. ^ Glenn AE, Bacon CW, Price R, Hanlin RT (1996). "Molecular phylogeny of Acremonium and its taxonomic implications". Mycologia. 88 (3): 369–383. doi:10.2307/3760878. JSTOR 3760878.
  9. ^ Spatafora JW, Sung GH, Sung JM, Hywel-Jones NL, White JF Jr (2007). "Phylogenetic evidence for an animal pathogen origin of ergot and the grass endophytes". Mol. Ecol. 16 (8): 1701–1711. Bibcode:2007MolEc..16.1701S. doi:10.1111/j.1365-294X.2007.03225.x. PMID 17402984. S2CID 3834591.
  10. ^ a b c d Schardl CL, Leuchtmann A, Spiering MJ (2004). "Symbioses of grasses with seedborne fungal endophytes". Annu Rev Plant Biol. 55: 315–340. doi:10.1146/annurev.arplant.55.031903.141735. PMID 15377223.
  11. ^ Freeman EM (1904). "The seed fungus of Lolium temulentum L., the darnel". Philosophical Transactions of the Royal Society of London, Series B. 196 (214–224): 1–27. doi:10.1098/rstb.1904.0001.
  12. ^ Blankenship JD, Spiering MJ, Wilkinson HH, Fannin FF, Bush LP, Schardl CL (2001). "Production of loline alkaloids by the grass endophyte, Neotyphodium uncinatum, in defined media". Phytochemistry. 58 (3): 395–401. Bibcode:2001PChem..58..395B. doi:10.1016/S0031-9422(01)00272-2. PMID 11557071.
  13. ^ Górzyńska, K.; et al. (2010). "An unusual BotanophilaEpichloë association in a population of orchardgrass (Dactylis glomerata) in Poland". Journal of Natural History. 44 (45–46): 2817–24. doi:10.1111/j.1570-7458.2006.00518.x. S2CID 85111726.
  14. ^ Schardl CL, Craven KD, Speakman S, Stromberg A, Lindstrom A, Yoshida R (2008). "A novel test for host-symbiont codivergence indicates ancient origin of fungal endophytes in grasses". Syst. Biol. 57 (3): 483–498. arXiv:q-bio/0611084. doi:10.1080/10635150802172184. PMID 18570040. S2CID 2703622.
  15. ^ Tan YY, Spiering MJ, Scott V, Lane GA, Christensen MJ, Schmid J (2001). "In planta regulation of extension of an endophytic fungus and maintenance of high metabolic rates in its mycelium in the absence of apical extension". Appl. Environ. Microbiol. 67 (12): 5377–5383. Bibcode:2001ApEnM..67.5377T. doi:10.1128/AEM.67.12.5377-5383.2001. PMC 93319. PMID 11722882.
  16. ^ Christensen MJ, Bennett RJ, Schmid J (2002). "Growth of Epichloë/Neotyphodium and p-endophytes in leaves of Lolium and Festuca grasses". Mycol. Res. 96: 93–106. doi:10.1017/S095375620100510X.
  17. ^ Christensen MJ, Bennett RJ, Ansari HA, Koga H, Johnson RD, Bryan GT, Simpson WR, Koolaard JP, Nickless EM, Voisey CR (2008). "Epichloë endophytes grow by intercalary hyphal extension in elongating grass leaves". Fungal Genet. Biol. 45 (2): 84–93. doi:10.1016/j.fgb.2007.07.013. PMID 17919950.
  18. ^ Tanaka A, Christensen MJ, Takemoto D, Park P, Scott B (2006). "Reactive oxygen species play a role in regulating a fungus-perennial ryegrass mutualistic interaction". Plant Cell. 18 (4): 1052–1066. doi:10.1105/tpc.105.039263. PMC 1425850. PMID 16517760.
  19. ^ Takemoto D, Tanaka A, Scott B (2006). "A p67Phox-like regulator is recruited to control hyphal branching in a fungal-grass mutualistic symbiosis". Plant Cell. 18 (10): 2807–2821. doi:10.1105/tpc.106.046169. PMC 1626622. PMID 17041146.
  20. ^ Tsai HF, Liu JS, Staben C, Christensen MJ, Latch GC, Siegel MR, Schardl CL (1994). "Evolutionary diversification of fungal endophytes of tall fescue grass by hybridization with Epichloë species". Proc. Natl. Acad. Sci. USA. 91 (7): 2542–2546. Bibcode:1994PNAS...91.2542T. doi:10.1073/pnas.91.7.2542. PMC 43405. PMID 8172623.
  21. ^ Moon CD, Craven KD, Leuchtmann A, Clement SL, Schardl CL (2004). "Prevalence of interspecific hybrids amongst asexual fungal endophytes of grasses". Mol Ecol. 13 (6): 1455–1467. Bibcode:2004MolEc..13.1455M. doi:10.1111/j.1365-294X.2004.02138.x. PMID 15140090. S2CID 11295842.
  22. ^ a b c d e f Bush LP, Wilkinson HH, Schardl CL (1997). "Bioprotective Alkaloids of Grass-Fungal Endophyte Symbioses". Plant Physiol. 114 (1): 1–7. doi:10.1104/pp.114.1.1. PMC 158272. PMID 12223685.
  23. ^ Scott B (2001). "Epichloë endophytes: fungal symbionts of grasses". Curr. Opin. Microbiol. 4 (4): 393–398. doi:10.1016/S1369-5274(00)00224-1. PMID 11495800.
  24. ^ Roberts, C.A.; West, C.P.; Spiers, D.E., eds. (2005). Neotyphodium in Cool-Season Grasses. Blackwell. ISBN 978-0-8138-0189-6.
  25. ^ a b Schardl CL, Panaccione DG, Tudzynski P (2006). Ergot alkaloids – biology and molecular biology. Vol. 63. pp. 45–86. doi:10.1016/S1099-4831(06)63002-2. ISBN 9780124695634. PMID 17133714. {{cite book}}: |journal= ignored (help)
  26. ^ Young CA, Felitti S, Shields K, Spangenberg G, Johnson RD, Bryan GT, Saikia S, Scott B (2006). "A complex gene cluster for indole-diterpene biosynthesis in the grass endophyte Neotyphodium lolii". Fungal Genet Biol. 43 (10): 679–693. doi:10.1016/j.fgb.2006.04.004. PMID 16765617.
  27. ^ a b Tanaka A, Tapper BA; Popay A, Parker; EJ, Scott B (2005). "A symbiosis expressed non-ribosomal peptide synthetase from a mutualistic fungal endophyte of perennial ryegrass confers protection to the symbiotum from insect herbivory". Mol. Microbiol. 57 (4): 1036–1050. doi:10.1111/j.1365-2958.2005.04747.x. PMID 16091042. S2CID 23657680.
  28. ^ a b c Smith, C. Michael; Clement, Stephen L. (2012-01-07). "Molecular Bases of Plant Resistance to Arthropods". Annual Review of Entomology. 57 (1). Annual Reviews: 309–328. doi:10.1146/annurev-ento-120710-100642. ISSN 0066-4170. PMID 21910639.
  29. ^ a b Schardl CL, Grossman RB, Nagabhyru P, Faulkner JR, Mallik UP (2007). "Loline alkaloids: currencies of mutualism". Phytochemistry. 68 (7): 980–996. Bibcode:2007PChem..68..980S. doi:10.1016/j.phytochem.2007.01.010. PMID 17346759.
  30. ^ Blankenship JD, Houseknecht JB, Pal S, Bush LP, Grossman RB, Schardl CL (2005). "Biosynthetic precursors of fungal pyrrolizidines, the loline alkaloids". ChemBioChem. 6 (6): 1016–1022. doi:10.1002/cbic.200400327. PMID 15861432. S2CID 13461396.
  31. ^ Zhang, DX, Nagabhyru, P, Schardl CL (2009). "Regulation of a chemical defense against herbivory produced by symbiotic fungi in grass plants". Plant Physiology. 150 (2): 1072–1082. doi:10.1104/pp.109.138222. PMC 2689992. PMID 19403726.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  32. ^ Gonthier DJ, Sullivan TJ, Brown KL, Wurtzel B, Lawal R, VandenOever K, Buchan Z, Bultman TL (2008). "Stroma-forming endophyte Epichloe glyceriae provides wound-inducible herbivore resistance to its grass host". Oikos. 117 (4): 629–633. doi:10.1111/j.0030-1299.2008.16483.x.
  33. ^ Barker GM; Patchett BJ; Cameron NE (2014). "Epichloë uncinata infection and loline content afford Festulolium grasses protection from black beetle (Heteronychus arator). Landcare Research, Hamilton, New Zealand & Cropmark Seeds Ltd, Christchurch, New Zealand 20 Dec 2014". New Zealand Journal of Agricultural Research. 58: 35–56. doi:10.1080/00288233.2014.978480. S2CID 85409823.
  34. ^ Ewald PW (1987). "Transmission modes and evolution of the parasitism-mutualism continuum". Ann NY Acad Sci. 503 (1): 295–306. Bibcode:1987NYASA.503..295E. doi:10.1111/j.1749-6632.1987.tb40616.x. PMID 3304078. S2CID 39350499.
  35. ^ Malinowski DP, Belesky DP (2000). "Adaptations of endophyte-infected cool-season grasses to environmental stresses: mechanisms of drought and mineral stress tolerance". Crop Sci. 40 (4): 923–940. doi:10.2135/cropsci2000.404923x.
  36. ^ Saikkonen K, Ion D, Gyllenberg M (2002). "The persistence of vertically transmitted fungi in grass metapopulations". Proc Biol Sci. 269 (1498): 1397–1403. doi:10.1098/rspb.2002.2006. PMC 1691040. PMID 12079664.
  37. ^ Saikkonen K, Lehtonen P, Helander M, Koricheva J, Faeth SH (2006). "Model systems in ecology: dissecting the endophyte-grass literature". Trends Plant Sci. 11 (9): 428–433. doi:10.1016/j.tplants.2006.07.001. PMID 16890473.
  38. ^ Clay K, Holah J, Rudgers JA (2005). "Herbivores cause a rapid increase in hereditary symbiosis and alter plant community composition". Proc. Natl. Acad. Sci. USA. 102 (35): 12465–12470. Bibcode:2005PNAS..10212465C. doi:10.1073/pnas.0503059102. PMC 1194913. PMID 16116093.
  39. ^ Kohn S, Hik DS (2007). "Herbivory mediates grass-endophyte relationships". Ecology. 88 (11): 2752–2757. Bibcode:2007Ecol...88.2752K. doi:10.1890/06-1958.1. PMID 18051643.
  40. ^ Granath G, Vicari M, Bazely DR, Ball JP, Puentes A, Rakocevic T (2007). "Variation in the abundance of fungal endophytes in fescue grasses along altitudinal and grazing gradients". Ecography. 30 (3): 422–430. Bibcode:2007Ecogr..30..422G. doi:10.1111/j.0906-7590.2007.05027.x.
  41. ^ Hahn H, McManus MT, Warnstorff K, Monahan BJ, Young CA, Davies E, Tapper BA, Scott, B (2007). "Neotyphodium fungal endophytes confer physiological protection to perennial ryegrass (Lolium perenne L.) subjected to a water deficit". Environ. Exp. Bot. 63 (1–3): 183–199. doi:10.1016/j.envexpbot.2007.10.021.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  42. ^ Hunt MG.; Rasmussen S; Newton PCD; Parsons AJ; Newman JA (2005). "Near-term impacts of elevated CO2, nitrogen and fungal endophyte-infection on Lolium perenne L. growth, chemical composition and alkaloid production". Plant Cell Environ. 28 (11): 1345–1354. doi:10.1111/j.1365-3040.2005.01367.x.