Neotyphodium 893313 225903866 2008-07-15T23:07:13Z Malljaja 3242335 /* Effects on the grass plant and on herbivores */ fixed doi {{Taxobox | name = ''Neotyphodium'' | regnum = [[Fungus|Fungi]] | divisio = [[Ascomycota]] | classis = [[Ascomycetes]] | subclassis = [[Sordariomycetes]] | ordo = [[Hypocreales]] | familia = [[Clavicipitaceae]] | genus = ''Neotyphodium'' }} '''''Neotyphodium''''' is a form [[genus]] containing species of [[endophytic]] [[fungi]]. These endophytes are [[asexual reproduction | asexual]], seed-borne [[symbiont]]s of cool-season [[grass]]es, and grow intercellularly throughout the aerial tissues of their [[host (biology)|host]]s, including shoot apical [[meristem]]s, leaf sheaths and blades, inflorescences, seeds and embryos.<ref name="Roberts">{{cite book| author = Roberts CA, West CP, Spiers DE, eds | title = Neotyphodium in Cool-Season Grasses|year = 2005|publisher = Blackwell|id = ISBN 978-0813801896}}</ref> ==Taxonomic considerations== ''Neotyphodium'' species are closely related to [[teleomorph]]ic species of the genus ''[[Epichloë]]'', from which many have evolved by processes involving interspecific hybridization.<ref name="Tsai">{{cite journal|author=Tsai HF, Liu JS, Staben C, Christensen MJ, Latch GC, Siegel MR, Schardl CL|year= 1994|title=Evolutionary diversification of fungal endophytes of tall fescue grass by hybridization with ''Epichloë'' species|journal= Proc. Natl. Acad. Sci. USA|volume=91|pages= 2542–2546|pmid=8172623|doi=10.1073/pnas.91.7.2542}}</ref>. 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.<ref name="Tsai"/><ref name="Moon">{{cite journal|author=Moon CD, Craven KD, Leuchtmann A, Clement SL, Schardl CL|year=2004|title=Prevalence of interspecific hybrids amongst asexual fungal endophytes of grasses|journal=Molec Ecol|volume=13|pages=1455–1467|pmid=15140090|doi=10.1111/j.1365-294X.2004.02138.x}}</ref> Hence, the form genus ''Neotyphodium'' is very closely associated with the [[teleomorph]]ic genus ''[[Epichloë]]''.<ref name="Glenn">{{cite journal|author=Glenn AE, Bacon CW, Price R, Hanlin RT|year=1996|title=Molecular phylogeny of ''Acremonium'' and its taxonomic implications|journal=Mycologia|volume=88|pages=369–383|doi=10.2307/3760878}}</ref> In keeping with the code of botanical nomenclature, the form genus refers to the asexual spore or vegetative state, and the [[teleomorph]]ic genus refers to the sexual state. ==Life cycle== 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. <ref name="Schardl">{{cite journal|author=Schardl CL, Leuchtmann A, Spiering MJ|year=2004|title=Symbioses of grasses with seedborne fungal endophytes|journal=Annu Rev Plant Biol|volume=55|pages=315–340|pmid=15377223|doi=10.1146/annurev.arplant.55.031903.141735}}</ref> Manifestation of the sexual state - which only occurs in ''Epichloë'' fungi — causes [[choke disease]], a condition in which grass [[inflorescence]]s are engulfed by rapid fungal outgrowth forming a stroma. The fungal stroma suppresses host seed production and culminates in the ejection of meiospores ([[ascospore]]s) that mediate horizontal (contagious) transmission of the fungus to new plants.<ref name="Schardl"> 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 ''Neotyphodium'' species 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 <ref name="Blankenship2001">{{cite journal|author=Blankenship JD, Spiering MJ, Wilkinson HH, Fannin FF, Bush LP, Schardl CL|year=2001|title=Production of loline alkaloids by the grass endophyte, ''Neotyphodium uncinatum'', in defined media|journal=Phytochemistry|volume=58|pages=395–401|pmid=11557071|doi=10.1016/S0031-9422(01)00272-2}}</ref>. ==Coevolution and growth synchrony with grass hosts== ''Neotyphodium'' (and ''Epichloë'') endophytes 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 [[Pooideae|pooid]] grasses. This is suggested by [[Phylogeny|phylogenetic]] studies indicating preponderance of [[cophylogeny]] of ''Neotyphodium''/''Epichloë'' species with the grass hosts they inhabit. <ref name="Schardl et al 2008">{{cite journal|author=Schardl CL, Craven KD, Speakman S, Stromberg A, Lindstrom A, Yoshida R.|year=2008|title=A novel test for host-symbiont codivergence indicates ancient origin of fungal endophytes in grasses.|journal=Syst Biol.|volume=57|pages=483-498|pmid= 18570040|doi=10.1080/10635150802172184}}</ref> Growth of the fungal symbiont is very tightly regulated within its grass host, indicated by a largely unbranched [[mycelium|mycelial]] morphology and remarkable [[synchrony]] of [[grass leaf]] and [[Hypha|hyphal]] extension of the fungus; <ref name="Tan et al 2001">{{cite journal|author=Tan YY, Spiering MJ, Scott V, Lane GA, Christensen MJ, Schmid J.|year=2001|title=In planta regulation of extension of an endophytic fungus and maintenance of high metabolic rates in its mycelium in the absence of apical extension|journal=Appl. Environ. Microbiol.|volume=67|pages=5377-5383|pmid= 11722882|doi=10.1128/AEM.67.12.5377-5383.2001}}</ref><ref name="Christensen et al 2002">{{cite journal|author=Christensen MJ, Bennett RJ, Schmid J|year=2002|title=Growth of ''Epichloë/Neotyphodium'' and p-endophytes in leaves of ''Lolium'' and ''Festuca'' grasses|journal=Mycol. Res.|volume=96|pages=93-106|doi=10.1017/S095375620100510X}}</ref> 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. <ref name="Christensen et al 2008">{{cite journal|author=Christensen MJ, Bennett RJ, Ansari HA, Koga H, Johnson RD, Bryan GT, Simpson WR, Koolaard JP, Nickless EM, Voisey CR|year=2008|title=Epichloë endophytes grow by intercalary hyphal extension in elongating grass leaves|journal=Fung. Genet. Biol.|volume=45|pages=84-93|pmid=17919950|doi=10.1016/j.fgb.2007.07.013}}</ref> A complex [[NADPH oxidase]] enzyme-based [[Reactive oxygen species|ROS]]-generating system in the endophyte is indispensable for maintenance of this growth synchrony, since [[Gene deletion|deletion]] of genes encoding these enzymes in the endophyte ''Epichloë festucae'' causes severely disordered fungal growth in grass tissues and even death of the grass plant.<ref name="Tanaka et al 2006">{{cite journal|author=Tanaka A, Christensen MJ, Takemoto D, Park P, Scott B|year=2006|title=Reactive oxygen species play a role in regulating a fungus-perennial ryegrass mutualistic interaction|journal=Plant Cell|volume=18|pages=1052-1066|pmid=16517760|doi=10.1105/tpc.105.039263}}</ref><ref name="Takemoto et al 2006">{{cite journal|author=Takemoto D, Tanaka A, Scott B|year=2006|title=A p67Phox-like regulator is recruited to control hyphal branching in a fungal-grass mutualistic symbiosis|journal=Plant Cell|volume=18|pages=2807-2821|pmid=17041146|doi=10.1105/tpc.106.046169}}</ref> ==Effects on the grass plant and on herbivores== It has been proposed that vertically transmitted [[symbiont]]s should evolve to be [[Mutualism|mutualists]] since their reproductive [[fitness (biology)|fitness]] is intimately tied to that of their hosts.<ref name="Ewald1987">{{cite journal|author=Ewald PW|year=1987|title=Transmission modes and evolution of the parasitism-mutualism continuum|journal=Ann NY Acad Sci|volume=503|pages=295–306|pmid=3304078|doi=10.1111/j.1749-6632.1987.tb40616.x}}</ref> In fact, some positive effects of ''Neotyphodium'' species on their host plants include increased growth, drought tolerance, and [[herbivore]] and [[pathogen]] resistance.<ref name="Schardl"/><ref name="Malinowski and Belesky">{{cite journal|author=Malinowski DP, Belesky DP|year= 2000|title=Adaptations of endophyte-infected cool-season grasses to environmental stresses: mechanisms of drought and mineral stress tolerance|journal= Crop Sci.|volume=40|pages=923–940}}</ref> Resistance against herbivores has been attributed to endophyte-produced [[alkaloids]].<ref name="Bush">{{cite journal|author=Bush LP, Wilkinson HH, Schardl CL|year= 1997|title=Bioprotective Alkaloids of Grass-Fungal Endophyte Symbioses|journal= Plant Physiol.|volume=114|pages= 1–7|pmid=12223685}}</ref> Although grass-endophyte 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.<ref name="Saikkonen">{{cite journal|author=Saikkonen K, Ion D, Gyllenberg M|year=2002|title=The persistence of vertically transmitted fungi in grass metapopulations|journal=Proc Biol Sci|volume=269|pages=1397–1403|pmid= 12079664|doi=10.1098/rspb.2002.2006}}</ref> Due to the relatively large number of grass species harboring endophytes and the variety of environments in which they occur, the mechanisms underlying beneficial or antagonstic outcomes of ''Neotyphodium''-grass symbioses are difficult to delineate in natural and also agricultural environments.<ref name="Schardl"/><ref name="Saikkonen al2006">{{cite journal|author=Saikkonen K, Lehtonen P, Helander M, Koricheva J, Faeth SH|year=2006|title=Model systems in ecology: dissecting the endophyte-grass literature|journal= Trends Plant Sci|volume=11|pages= 428-433|pmid=16890473|doi=10.1016/j.tplants.2006.07.001 }}</ref> Some studies suggest a relationship between grazing by herbivores and increased endophyte infection <ref name="Clay et al2005">{{cite journal|author=Clay K, Holah J, Rudgers JA|year=2005|title=Herbivores cause a rapid increase in hereditary symbiosis and alter plant community composition|journal= Proc. Natl. Acad. Sci. USA|volume=102|pages= 12465-12470|pmid=16116093|doi=10.1073/pnas.0503059102}}</ref><ref name="Kohn et al2007">{{cite journal|author=Kohn S, Hik DS|year=2007|title=Herbivory mediates grass-endophyte relationships|journal= Ecology|volume=88|pages= 2752-2757|pmid=18051643|doi=10.1890/06-1958.1}}</ref>, whereas others indicate a complex interplay between plant species and fungal symbionts in response to herbivory or environmental conditions. <ref name="Granath et al2007">{{cite journal|author=Granath G, Vicari M, Bazely DR, Ball JP, Puentes A, Rakocevic T|year=2007|title= Variation in the abundance of fungal endophytes in fescue grasses along altitudinal and grazing gradients|journal= Ecography|volume=3|pages=422-430|doi=10.1111/j.0906-7590.2007.05027.x}}</ref> The strong anti-herbivore activities of the ''Neotyphodium'' endophyte alkaloids <ref name="Bush"/><ref name="Tanaka"/> and relatively moderate direct effects of the endophytes on plant growth and physiology <ref name="Hahn et al2008">{{cite journal|author=Hahn H, McManus MT, Warnstorff K, Monahan BJ, Young CA, Davies E, Tapper BA, Scott, B|year=2007|title=''Neotyphodium'' fungal endophytes confer physiological protection to perennial ryegrass (''Lolium perenne'' L.) subjected to a water deficit|journal= Env. Exp. Bot.|volume=63|pages=183-199|doi=10.1016/j.envexpbot.2007.10.021}}</ref><ref name="Hunt et al2005">{{cite journal|author=Hunt MG., Rasmussen S, Newton PCD, Parsons AJ, Newman JA|year=2005|title= Near-term impacts of elevated CO2, nitrogen and fungal endophyte-infection on ''Lolium perenne'' L. growth, chemical composition and alkaloid production|journal= Plant Cell Environ.|volume=28|pages=1345-1354|doi=10.1111/j.1365-3040.2005.01367.x}}</ref> suggest that the endophyte-produced alkaloids play a major role in the persistence of the symbiosis. ==''Neotyphodium'' alkaloids== [[Ergoline]] alkaloids (which are ergot alkaloids, named after the [[ergot]] fungus, ''[[Claviceps purpurea]]'', a close relative of the ''Neotyphodium/Epichloë'' endophytes) are characterized by a ring system derived from 4-[[prenyl]] [[tryptophan]].<ref name="Schardl2006">{{cite journal|author=Schardl CL, Panaccione DG, Tudzynski P|year=2006|title=Ergot alkaloids – biology and molecular biology|journal=The Alkaloids: Chemistry and Biology|volume=63|pages=45–86|pmid=17133714|doi=10.1016/S1099-4831(06)63002-2}}</ref> Among the most abundant ergot alkaloids in endophyte-symbiotic grasses is ergovaline, comprising an [[ergoline]] [[moiety]] attached to a bicyclic [[tripeptide]] containing the [[amino acids]], <small>L</small>-[[proline]], <small>L</small>[[alanine]], and <small>L</small>-[[valine]]. Key genes and enzymes for ergot alkaloid biosynthesis have been identified in ''Neotyphodium'' and include ''dmaW'', encoding [[Tryptophan dimethylallyltransferase|dimethylallyl-tryptophan synthase]] and ''lpsA'', a [[Nonribosomal peptide|non-ribosomal peptide synthetase]]. <ref name="Schardl2006"> Another group of endophyte alkaloids are the [[indole]]-[[diterpenoid]]s, such as lolitrem B, which are produced from the activity of several enzymes, including [[prenyltransferase]]s and various [[monooxygenase]]s.<ref name="Young2006">{{cite journal|author=Young CA, Felitti S, Shields K, Spangenberg G, Johnson RD, Bryan GT, Saikia S, Scott B|year=2006|title=A complex gene cluster for indole-diterpene biosynthesis in the grass endophyte ''Neotyphodium lolii''|journal=Fung Genet Biol|volume=43|pages=679–693|pmid= 16765617|doi=10.1016/j.fgb.2006.04.004}}</ref> Both the ergoline and indole-diterpenoid alkaloids have [[biological activity]] against mammalian [[herbivores]], and also activity against some insects. Peramine is a pyrrolopyrazine alkaloid thought to be biosynthesized from the [[guanidine|guanidinium]]-group-containing amino acid, <small>L</small>-[[arginine]], and pyrrolidine-5-[[carboxylate]], a precursor of <small>L</small>-[[proline]],<ref name="Tanaka">{{cite journal|author=Tanaka A, Tapper BA, Popay A, Parker, EJ, Scott B |year= 2005|title=A symbiosis expressed non-ribosomal peptide synthetase from a mutualistic fungal endophyte of perennial ryegrass confers protection to the symbiotum from insect herbivory|journal=Mol. Microbiol.|volume=57|pages= 1036–1050|pmid=16091042|doi=10.1111/j.1365-2958.2005.04747.x}}</ref> and is an insect-feeding deterrent. The loline alkaloids are 1-aminopyrrolizidines with an oxygen atom linking bridgehead carbons 2 and 7, and are biosynthesized from the [[amino acids]], <small>L</small>-proline and <small>L</small>-[[homoserine]].<ref name="Blankenship">{{cite journal|author=Blankenship JD, Houseknecht JB, Pal S, Bush LP, Grossman RB, Schardl CL|year= 2005|title=Biosynthetic precursors of fungal pyrrolizidines, the loline alkaloids|journal=Chembiochem|volume=6|pages=1016–1022|pmid=15861432|doi=10.1002/cbic.200400327}}</ref> The lolines have [[insecticidal]] and insect-deterrent activities comparable to [[nicotine]]. Many, but not all, ''Neotyphodium'' species produce up to three classes of these [[alkaloid]]s. ==Species== * ''[[Neotyphodium aotearoae]]'' * ''[[Neotyphodium australiense]]'' * ''[[Neotyphodium chilense]]'' * ''[[Neotyphodium chisosum]]'' * ''[[Neotyphodium coenophialum]]'' * ''[[Neotyphodium gansuense]]'' * ''[[Neotyphodium huerfanum]]'' * ''[[Neotyphodium lolii]]'' * ''[[Neotyphodium melicicola]]'' * ''[[Neotyphodium occultans]]'' * ''[[Neotyphodium siegelii]]'' * ''[[Neotyphodium starrii]]'' * ''[[Neotyphodium tembladerae]]'' * ''[[Neotyphodium typhinum]]'' * ''[[Neotyphodium uncinatum]]'' ==References== <references /> [[Category:Sordariomycetes]] [[Category:Fungi of New Zealand]]