Neotyphodium

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Neotyphodium
Neotyphodium coenophialum.jpg
Neotyphodium coenophialum
Scientific classification
Kingdom: Fungi
Division: Ascomycota
Class: Ascomycetes
Subclass: Sordariomycetes
Order: Hypocreales
Family: Clavicipitaceae
Genus: Neotyphodium
Glenn, C.W. Bacon & Hanlin (1996)
Type genus
Neotyphodium coenophialum
(Morgan-Jones & W. Gams) Glenn, C.W. Bacon & Hanlin (1996)

Neotyphodium is a form genus containing species of endophytic fungi. These endophytes are asexual, seed-borne symbionts of cool-season grasses, and grow intercellularly throughout the aerial tissues of their hosts, including shoot apical meristems, leaf sheaths and blades, inflorescences, seeds and embryos. The Neotyphodium endophytes produce at least four different classes of compounds with various biological activities (toxicity or feeding deterrence) against insect and mammalian herbivores.[1]

Taxonomic considerations[edit]

Neotyphodium species (with the likely exception of N. chilense) are closely related to teleomorphic species of the genus Epichloë, from which many have evolved by processes involving interspecific hybridization.[2] Molecular phylogenetic evidence demonstrates that asexual Neotyphodium species are derived either from individual Epichloë species, or more commonly, from hybrids with at least two ancestral Epichloë species.[2][3] Hence, the form genus Neotyphodium is very closely associated with the teleomorphic genus Epichloë.[4] In keeping with the code of botanical nomenclature, the form genus refers to the asexual spore or vegetative state, and the teleomorphic genus refers to the sexual state. Because of their close relationships and shared biological properties, members of these two genera are collectively called 'epichloae' (singular = 'epichloë').

Life cycle[edit]

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, all Neotyphodium and some Epichloë species infect new grass plants solely by growing into the seeds of their grass hosts, and infecting the growing seedling.[5][6] 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.[5] 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.[7]

Coevolution and growth synchrony with grass hosts[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 preponderance of codivergence of Neotyphodium/Epichloë species with the grass hosts they inhabit.[8] 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;[9][10] 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.[11] A complex NADPH oxidase enzyme-based ROS-generating system in epichloae 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.[12][13]

Effects on the grass plant and on herbivores[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.[14] In fact, some positive effects of epichloae on their host plants include increased growth, drought tolerance, and herbivore and pathogen resistance.[5][15] Resistance against herbivores has been attributed to alkaloids produced by the symbiotic epichloae.[16] 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.[17]

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.[5][18] Some studies suggest a relationship between grazing by herbivores and increased epichloë infestation of the grasses on which they feed,[19][20] whereas others indicate a complex interplay between plant species and fungal symbionts in response to herbivory or environmental conditions.[21] The strong anti-herbivore activities of several bioactive compounds produced by the epichloae [16][22] and relatively modest direct effects of the epichloae on plant growth and physiology[23][24] suggest that these compounds play a major role in the persistence of the symbiosis.

Bioactive compounds[edit]

Many Neotyphodium endophytes produce a diverse range of natural product compounds with biological activities against a broad range of herbivores.[16][25] 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.[26] 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.[26]

N-formylloline, an insecticidal alkaloid produced in several Neotyphodium–grass symbiota.

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.[27] Both the ergoline and indole-diterpenoid alkaloids have biological activity against mammalian herbivores, and also activity against some insects.[16] 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,[22] and is an insect-feeding deterrent. The loline alkaloids [28] 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.[29] The lolines have insecticidal and insect-deterrent activities comparable to nicotine.[28] Loline accumulation is strongly induced in young growing tissues[30] or by damage to the plant-fungus symbiotum.[31] Many, but not all, epichloae produce up to three classes of these alkaloids in various combinations and amounts.[16]

Species[edit]

References[edit]

  1. ^ Roberts CA, West CP, Spiers DE, eds (2005). Neotyphodium in Cool-Season Grasses. Blackwell. ISBN 978-0-8138-0189-6. 
  2. ^ a b 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. doi:10.1073/pnas.91.7.2542. PMC 43405. PMID 8172623. 
  3. ^ Moon CD, Craven KD, Leuchtmann A, Clement SL, Schardl CL (2004). "Prevalence of interspecific hybrids amongst asexual fungal endophytes of grasses". Molec Ecol 13 (6): 1455–1467. doi:10.1111/j.1365-294X.2004.02138.x. PMID 15140090. 
  4. ^ Glenn AE, Bacon CW, Price R, Hanlin RT (1996). "Molecular phylogeny of Acremonium and its taxonomic implications". Mycologia (Mycological Society of America) 88 (3): 369–383. doi:10.2307/3760878. JSTOR 3760878. 
  5. ^ 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. 
  6. ^ Freeman EM (1904). "The seed fungus of Lolium temulentum L., the darnel". Philosophical Transactions of the Royal Society of London, Series B 196: 1–27. doi:10.1098/rstb.1904.0001. 
  7. ^ 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. doi:10.1016/S0031-9422(01)00272-2. PMID 11557071. 
  8. ^ 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. doi:10.1080/10635150802172184. PMID 18570040. 
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  12. ^ 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. 
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  14. ^ Ewald PW (1987). "Transmission modes and evolution of the parasitism-mutualism continuum". Ann NY Acad Sci 503: 295–306. doi:10.1111/j.1749-6632.1987.tb40616.x. PMID 3304078. 
  15. ^ 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: 923–940. doi:10.2135/cropsci2000.404923x. 
  16. ^ a b c d e Bush LP, Wilkinson HH, Schardl CL (1997). "Bioprotective Alkaloids of Grass-Fungal Endophyte Symbioses". Plant Physiol. 114 (1): 1–7. PMC 158272. PMID 12223685. 
  17. ^ 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. 
  18. ^ 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. 
  19. ^ 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. doi:10.1073/pnas.0503059102. PMC 1194913. PMID 16116093. 
  20. ^ Kohn S, Hik DS (2007). "Herbivory mediates grass-endophyte relationships". Ecology 88 (11): 2752–2757. doi:10.1890/06-1958.1. PMID 18051643. 
  21. ^ 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 3: 422–430. doi:10.1111/j.0906-7590.2007.05027.x. 
  22. ^ 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. 
  23. ^ 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". Env. Exp. Bot. 63: 183–199. doi:10.1016/j.envexpbot.2007.10.021. 
  24. ^ 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: 1345–1354. doi:10.1111/j.1365-3040.2005.01367.x. 
  25. ^ 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. 
  26. ^ a b Schardl CL, Panaccione DG, Tudzynski P (2006). "Ergot alkaloids – biology and molecular biology". The Alkaloids: Chemistry and Biology 63: 45–86. doi:10.1016/S1099-4831(06)63002-2. PMID 17133714. 
  27. ^ 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". Fung Genet Biol 43 (10): 679–693. doi:10.1016/j.fgb.2006.04.004. PMID 16765617. 
  28. ^ a b Schardl CL, Grossman RB, Nagabhyru P, Faulkner JR, Mallik UP (2007). "Loline alkaloids: currencies of mutualism". Phytochemistry 68 (7): 980–996. doi:10.1016/j.phytochem.2007.01.010. PMID 17346759. 
  29. ^ 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. 
  30. ^ 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. 
  31. ^ 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: 629–633. doi:10.1111/j.0030-1299.2008.16483.x. 

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