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2019 | 72 | 2 |
Tytuł artykułu

Epichloe (formerly Neotyphodium) fungal endophytes increase adaptation of cool-season perennial grasses to environmental stresses

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PL
Epichloe (dawniej Neotyphodium) grzybowe endofyty zwiększają adaptacje traw zimotrwałych do stresów środowiskowych
Języki publikacji
EN
Abstrakty
EN
Many cool-season grass species have evolved with asexual, nonsymptomatic fungal endophytes of the genus Epichloë (formerly Neotyphodium) of the family Clavicipitaceae. These associations range from parasitic to mutualistic and have dramatic effects on grass host chemistry, increasing resistance to abiotic (drought, soil mineral imbalance) and biotic (vertebrate and invertebrate herbivory, nematodes, plant pathogens, plant competition) stresses. Native endophyte strains produce a range of bioprotective alkaloid and other nonalkaloid secondary compounds, several of them known to have detrimental effects on grazing animals. In the past two decades, epichloid endophyte strains have been selected with marginal or no capacity of producing ergot and/or lolitrem alkaloids. These novel endophyte strains have been introduced to several grass cultivars with the idea to increase grass host resistance to abiotic stresses without hindering grazing livestock, and abiotic stresses to ensure high competitive ability of symbiotic grass cultivars. In this presentation, we discuss mechanisms underlying the competitiveness of epichloid endophyte/grass associations and consequences of endophyte infection for grassland ecosystem functions.
PL
W trakcie ewolucji, wiele gatunków traw zimotrwałych ukształtowało symbiozy z bezpłciowymi, bezobjawowymi grzybowymi endofytami z rodzaju Epichloë (dawniej Neotyphodium ) z rodziny Clavicipitaceae. Zależności pomiędzy tymi organizmami obejmują zarówno relacje pasożytnicze jak i mutualistyczne, i mają ogromny wpływ na szlaki metaboliczne traw, np. zwiększają odporność na wiele stresów środowiskowych (susza, zaburzenia równowagi mineralnej w glebie) i biotycznych (uszkodzenia liści przez zwierzęta kręgowe i bezkręgowe, pasożytnicze nicienie, patogeny i konkurencję z innymi roślinami). Niektóre szczepy endofytów wytwarzają szereg alkaloidów i innych wtórnych związków chemicznych, które mogą mieć szkodliwy wpływ na zwierzęta wypasane na symbiotycznych trawach. W ciągu ostatnich dwóch dekad zostały wyizolowane szczepy endofytów, które nie produkują związków chemicznych szkodliwych dla zwierząt, tj. alkaloidy z grupy ergot czy lolitrem. Te nowe szczepy endofitów zostały wprowadzone do kilku odmian traw pastwiskowych z myślą o zwiększeniu ich odporności na stresy środo- wiskowe, ale bez negatywnego wpływu na wypasane zwierzęta hodowlane w celu zapewnienia wysokiej zdolności konkurowania symbiotycznych odmian traw z chwastami. W niniejszej pracy omawiamy mechanizmy odpowiedzialne za większą zdolność konkurencyjną symbiotycznych traw oraz konsekwencje tej symbiozy dla ekosystemów roślinnych.
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72
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2
Opis fizyczny
Article: 1767 [26 p.], ref.
Twórcy
  • Texas A&M AgriLife Research, P.O.Box 1658, 11708 Highway 70, South Vernon, TX 76384-1658, USA
autor
  • Division of Plant and Soil Sciences, West Virginia University, 1082 Agricultural Sciences Building, P.O.Box 6108, 101 Research Way, Morgantown, WV 26506-6108, USA
Bibliografia
  • Downie JA, Brewin NJ. Plant–microorganism symbiosis. In: Russo VEA, Cove DJ, Edgar LG, Jaenisch R, Salamini F, editors. Development. Genetics, epigenetics and environmental regulation. Berlin: Springer; 1999. p. 211–230. https://doi.org/10.1007/978-3-642-59828-9_14
  • Harley JL, Smith SE. Mycorrhizal symbiosis. London: Academic Press; 1983.
  • Wurzburger N, Miniat CF. Drought enhances symbiotic dinitrogen fixation and competitive ability of a temperate forest tree. Oecologia. 2014;174:1117–1126. https://doi.org/10.1007/s00442-013-2851-0
  • Moora M, Zobel M. Effect of arbuscular mycorrhiza on inter- and intraspecific competition of two grassland species. Oecologia. 1996;108:79–84. https://doi.org/10.1007/BF00333217
  • Leuchtmann A, Bacon CW, Schardl CL, White JF Jr, Tadych M. Nomenclatural realignment of Neotyphodium species with genus Epicholë. Mycologia. 2014;106:202–215. https://doi.org/10.3852/106.2.202
  • Morgan-Jones G, Gams W. 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. 1982;15:311–318.
  • Latch GCM, Christensen MJ. Ryegrass endophyte, incidence and control. New Zealand Journal of Agricultural Research. 1982;25:443–448. https://doi.org/10.1080/00288233.1982.10417910
  • Gams W, Petrini O, Schmidt D. Acremonium uncinatum, a new endophyte in Festuca pratensis. Mycotaxon. 1990;37:67–71.
  • Young CA, Hume DE, McCulley RL. Fungal endophytes of tall fescue and perennial ryegrass: pasture friend or foe? J Anim Sci. 2013;91:2379–2394. https://doi.org/10.2527/jas2012-5951
  • Moon CD, Craven KD, Leuchtmann A, Clement SL, Schardl CL. Prevalence of interspecific hybrids amongst asexual fungal endophytes of grasses. Mol Ecol. 2004;13:1455–1467. https://doi.org/10.1111/j.1365-294X.2004.02138.x
  • Selosse, MA, Schardl, CL. Fungal endophytes of grasses: hybrids rescued by vertical transmission? An evolutionary perspective. New Phytol. 2007;173:452–458. https://doi.org/10.1111/j.1469-8137.2007.01978.x
  • Tsai HF, Liu JS, Staben C, Christensen MJ, Latch GC, Siegel MR, et al. Evolutionary diversification of fungal endophytes of tall fescue grass by hybridization with Epichloë species. Proc Natl Acad Sci USA. 1994;91:2542–2546. https://doi.org/10.1073/pnas.91.7.2542
  • Norton MR, Malinowski DP, Volaire F. Plant drought survival under climate change and strategies to improve perennial grasses. A review. Agron Sustain Dev. 2016;36:29. https://doi.org/10.1007/s13593-016-0362-1
  • Christensen MJ, Leuchtmann A, Rowan DD, Tapper BA. Taxonomy of Acremonium endophytes of tall fescue (Festuca arundinacea), meadow fescue (F. pratensis), and perennial ryegrass (Lolium perenne). Mycol Res. 1993;97:1083–1092. https://doi.org/10.1016/S0953-7562(09)80509-1
  • Takach JE, Mittal S, Swoboda GA, Bright SK, Trammell MA, Hopkins AA, et al. Genotypic and chemotypic diversity of Neotyphodium endophytes in tall fescue from Greece. Appl Environ Microbiol. 2012;78:5501–5510. https://doi.org/10.1128/AEM.01084-12
  • Moon CD, Tapper BA, Scott B. Identification of Epichloë endophytes in planta by a microsatellite-based PCR fingerprinting assay with automated analysis. Appl Environ Microbiol. 1999;65:1268–1279.
  • Saikkonen K, Young CA, Helander M, Schardl CL. Endophytic Epichloë species and their grass hosts: from evolution to applications. Plant Mol Biol. 2016;6:665–675. https://doi.org/10.1007/s11103-015-0399-6
  • Saikkonen K, Ahlholm J, Helander M, Lehtimäki S, Niemeläinen O. Endophytic fungi in wild and cultivated grasses in Finland. Ecography. 2000;23:360–366. https://doi.org/10.1111/j.1600-0587.2000.tb00292.x
  • Song H, Nan Z. Origin, divergence, and phylogeny of asexual Epichloë endophyte in Elymus species from Western China. PLoS One. 2015;10:e0127096. https://doi.org/10.1371/journal.pone.0127096
  • Bastías DA, Martínez‐Ghersa MA, Newman JA, Card SD, Mace WJ, Gundel PE. The plant hormone salicylic acid interacts with the mechanism of anti‐herbivory conferred by fungal endophytes in grasses. Plant Cell Environ. 2018;41:395–405. https://doi.org/10.1111/pce.13102
  • Hamilton CE, Gundel PE, Helander M, Saikkonen K. Endophytic mediation of reactive oxygen species and antioxidant activity in plants: a review. Fungal Divers. 2012;54:1–10. https://doi.org/10.1007/s13225-012-0158-9
  • Saikkonen K, Gundel PE, Helander M. Chemical ecology mediated by fungal endophytes in grasses. J Chem Ecol. 2013;39:962–968. https://doi.org/10.1007/s10886-013-0310-3
  • Malinowski DP, Belesky DP. Adaptations of endophyte-infected cool-season grasses to environmental stresses: mechanisms of drought and mineral stress tolerance. Crop Sci. 2000;40:923–940. https://doi.org/10.2135/cropsci2000.404923x
  • Malinowski DP, Belesky DP. Ecological importance of Neotyphodium spp. grass endophytes in agroecosystems. Grassl Sci. 2006;52:1–14. https://doi.org/10.1111/j.1744-697X.2006.00041.x
  • Bacon CW, Hinton DM, Glenn AE. Endophytic niche and grass defense. In: White JF Jr, Torres MS, editors. Defensive mutualism in microbial symbiosis. Boca Raton, FL: CRC Press; 2009. p. 385–404. https://doi.org/10.1201/9781420069327.ch23
  • Huang WY, Cai YZ, Xing J, Corke H, Sun M. A Potential antioxidant resource: endophytic fungi from medicinal plants. Econ Bot. 2007;61:14–30. https://doi.org/10.1663/0013-0001(2007)61[14:APAREF]2.0.CO;2
  • White JF, Torres MS. Is plant endophyte-mediated defensive mutualism the result of oxidative stress protection? Physiol Plant. 2009;138:440–446. https://doi.org/10.1111/j.1399-3054.2009.01332.x
  • Qawasmeh A, Obied HK, Raman A, Wheatley W. Influence of fungal endophyte infection on phenolic content and antioxidant activity in grasses: Interaction between Lolium perenne and different strains of Neotyphodium lolii. Journal of Agriculture and Food Chemistry. 2012;60:3381–3388. https://doi.org/10.1021/jf204105k
  • Latch GCM, Christensen MJ, Samuels GJ. Five endophytes of Lolium and Festuca in New Zealand. Mycotaxon. 1984;20:535–550.
  • An ZQ, Siegel MR, Hollin W, Tsai HF, Schmidt D, Schardl CL. Relationships among non-Acremonium sp. fungal endophytes in five grass species. Appl Environ Microbiol. 1993;59:1540–1548.
  • Tadych M, White JF. Endophytic microbes. In: Schaechter M, editor. Eukaryotic microbes. San Diego, CA: Academic Press; 2012. p. 54–64.
  • Schmidt D. Effects of Acremonium uncinatum and a Phialophora-like endophyte on vigour, insect and disease resistance of meadow fescue. In: Hume DE, Latch GCM, Easton HS, editors. Proceedings of the 2nd International Symposium on Acremonium/Grass Interactions; 1993 Feb 4–6; Palmerson North, New Zealand. Palmerston North: AgResearch Grasslands Research Centre; 1993. p. 185–187.
  • Philipson MN. A symptomless endophyte of ryegrass (Lolium perenne) that spores on its host- a light microscope study. N Z J Bot. 1989;27:513–519. https://doi.org/10.1080/0028825X.1989.10414136
  • Naffaa W, Ravel C, Boyer N, Guillaumin JJ. Peroxidase activity of perennial ryegrass and tall fescue seedlings artificially infected with endophytes. Agronomie, EDP Sciences. 1999;19:611–619. https://doi.org/10.1051/agro:19990705
  • Philipson MN. Ultrastructure of the Gliocladium-like endophyte of perennial ryegrass (Lolium perenne L.). New Phytol. 1991;117:271–280. https://doi.org/10.1111/j.1469-8137.1991.tb04908.x
  • Siegel MR, Latch GCM. Expression of antifungal activity in agar culture by isolates of grass endophytes. Mycologia. 1991;83:525–537. https://doi.org/10.1080/00275514.1991.12026047
  • Malinowski D, Leuchtmann A, Schmidt D, Nösberger J. Growth and water status in meadow fescue is affected by Neotyphodium and Phialophora species endophytes. Agron J. 1997;89:673–678. https://doi.org/10.2134/agronj1997.00021962008900040021x
  • Tadych M, Ambrose KV, Bergen MS, Belanger FC, White JF. Taxonomic placement of Epichloë poae sp. nov. and horizontal dissemination to seedlings via conidia. Fungal Divers. 2012;54:117–131. https://doi.org/10.1007/s13225-012-0170-0
  • Clay K. Fungal endophytes of grasses – a defensive mutualism between plants and fungi. Ecology. 1988;69:10–16. https://doi.org/10.2307/1943155
  • Clay K. Defensive mutualism and grass endophytes: still valid after all these years? In: Torres M, White JF Jr, editors. Defensive mutualism in symbiotic association. Oxford: Taylor and Francis Publications; 2009. p. 9–20. https://doi.org/10.1201/9781420069327.ch2
  • Clay K, Holah J. Fungal endophyte symbiosis and plant diversity in successional fields. Science. 1999;285:1742–1744. https://doi.org/10.1126/science.285.5434.1742
  • Rudgers JA, Koslow JM, Clay K. Endophytic fungi alter relationships between diversity and ecosystem properties. Ecol Lett. 2004;7:42–51. https://doi.org/10.1046/j.1461-0248.2003.00543.x
  • Torres MS, White JF Jr. Grass endophyte-mediated plant stress tolerance: alkaloids and their functions. In: Seckbach J, Grube M, editors. Symbioses and stress. Dordrecht: Springer; 2010. p. 477–493. (Cellular Origin, Life in Extreme Habitats and Astrobiology; vol 17). https://doi.org/10.1007/978-90-481-9449-0_24
  • Schardl CL, Young CA, Faulkner JR, Florea S, Pan J. Chemotypic diversity of epichloae, fungal symbionts of grasses. Fungal Ecol. 2012;5:331–344. https://doi.org/10.1016/j.funeco.2011.04.005
  • Schardl CL, Florea S, Pan J, Nagabhyru P, Bec S, Calie PJ. The epichloae: alkaloid diversity and roles in symbiosis with grasses. Curr Opin Plant Biol. 2013;16:480–488. https://doi.org/10.1016/j.pbi.2013.06.012
  • Schardl CL, Grossman RB, Nagabhyru P, Faulkner JR, Mallik UP. Loline alkaloids: currencies of mutualism. Phytochemistry. 2007;68:980–996. https://doi.org/10.1016/j.phytochem.2007.01.010
  • Young CA, Schardl CL, Panaccione DG, Florea S, Takach JE, Charlton ND, et al. Genetics, genomics and evolution of ergot alkaloid diversity. Toxins. 2015;7:1273–1302. https://doi.org/10.3390/toxins7041273
  • Belesky DP, Stringer WC, Plattner RD. Influence of endophyte and water regime upon tall fescue accessions. II. Pyrrolizidine and ergopeptine alkaloids. Ann Bot. 1989;64:343–349. https://doi.org/10.1093/oxfordjournals.aob.a087850
  • Robbins JD, Wilkinson SR, Burdick D. Loline alkaloids of tall fescue seed and forage. In: Proceedings of the Fescue Toxicity Conference; 1973 May 31 – Jun 1; Lexington, KY, USA. Lexington, KY: University of Kentucky; 1993. p. 98–107
  • Ball OJ, Prestidge RA, Sprosen JM. Interrelationships between Acremonium lolii, peramine, and lolitrem B in perennial ryegrass. Appl Environ Microbiol. 1995;61:1527–1533.
  • Justus M, Witte L, Hartmann T. Levels and tissue distribution of loline alkaloids in endophyte‐infected Festuca pratensis. Phytochemistry. 1997;44:51–57. https://doi.org/10.1016/S0031-9422(96)00535-3
  • Ryan GD, Rasmussen S, Xue H, Parsons AJ, Newman JA. Metabolite analysis of the effects of elevated CO2 and nitrogen fertilization on the association between tall fescue (Schedonorus arundinaceus) and its fungal symbiont Neotyphodium coenophialum. Plant Cell Environ. 2014;37:204–212. https://doi.org/10.1111/pce.12146
  • Hennessy LM, Popay AJ, Finch SC, Clearwater MJ, Cave VM. Temperature and plant genotype alter alkaloid concentrations in ryegrass infected with an Epichloë endophyte and this affects an insect herbivore. Front Plant Sci. 2016;7:1097. https://doi.org/10.3389/fpls.2016.01097
  • Yoshihara T, Togiya S, Koshino H, Sakamura S, Shimanuki T, Sato T, et al. Three fungitoxic cyclopentanoidsesquiterpenes from stromata of Epichloë typhina. Tetrahedron Lett. 1985;26:5551–5554. https://doi.org/10.1016/S0040-4039(01)80885-6
  • Koshino, H, Terada S, Yoshihara T, Sakamura S, Shimanuki T, Sato T, et al. Three phenolic acid derivates from stromata of Epichloë typhina on Phleum pratense. Phytochemistry. 1988;27:1333–1338. https://doi.org/10.1016/0031-9422(88)80188-2
  • Koshino H, Yoshihara T, Sakamura S, Shimanuki T, Sato T, Tajimi A. A ring B aromatic sterol from stromata of Epichloë typhina. Phytochemistry. 1999;28:771–772. https://doi.org/10.1016/0031-9422(89)80112-8
  • Ju Y, Sacalis JN, Still CC. Bioactive flavonoids from endophyte-infected bluegrass (Poa ampla). Journal of Agriculture and Food Chemistry. 1998;46:3785–3788. https://doi.org/10.1021/jf980189m
  • Bacon CW, Porter JK, Robbins JD, Luttrell ES. Epichloë typhina from toxic tall fescue grasses. Appl Environ Microbiol. 1977;34:576–581.
  • Porter JK. Chemical constituents of grass endophytes. In: Bacon CW, White JF, Jr, editors. Biotechnology of endophytic fungi of grasses. Boca Raton, FL: CRC Press; 1994. p. 103–123.
  • Hoffmann A, Tscherter H. Isolierung von Lysergsaurealkaloiden aus der mexicanischen Zauberdroge “ololiuiqui” [Rivea corymbosa (L.) Hall.]. Experientia. 1960;16:414. https://doi.org/10.1007/BF02178840
  • Crosignani PG. Current treatment issues in female hyperprolactinaemia. European Journal of Obstetrics, Gynecology and Reproductive Biology. 2006;125:152–164. https://doi.org/10.1016/j.ejogrb.2005.10.005
  • Eich E, Pertz H. Antimicrobial and antitumor effects of ergot alkaloids and their derivatives. In: Kren V, Cvak L, editors. Ergot: the genus Claviceps. Amsterdam: Harwood Academic Publishers; 1999. p. 441–449.
  • Raisbeck MF, Rottinghaus GE, Kendall JD. Effects of naturally occurring mycotoxins on ruminants. In: Smith JE, Henderson RS, editors. Mycotoxins and animal foods. Boca Raton, FL: CRC Press; 1991. p. 647–677.
  • Thompson FN, Stuedemann JA. Pathophysiology of fescue toxicosis. Agriculture, Ecosystems and Environment. 1993;44:263–281. https://doi.org/10.1016/0167-8809(93)90050-Y
  • Tor-Agbidye J, Blythe LL, Craig AM. Correlation of endophyte toxins (ergovaline and lolitrem B) with clinical disease: fescue foot and perennial ryegrass staggers. Vet Hum Toxicol. 2001;43:140–146.
  • Spiers DE, Zhang Q, Eichen PA, Rottinghaus GE, Garner GB, Ellersieck MR. Temperature-dependent responses of rats to ergovaline derived from endophyte-infected tall fescue. J Anim Sci. 1995;73:1954–1961. https://doi.org/10.2527/1995.7371954x
  • Bush LP, Wilkinson HH, Schardl CL. Bioprotective alkaloids of grass–fungal endophyte symbioses. Plant Physiol. 1997;114:1–7. https://doi.org/10.1104/pp.114.1.1
  • Wilkinson HH, Siegel MR, Blankenship JD, Mallory AC, Bush LP, Schardl CL. Contribution of fungal loline alkaloids to protection from aphids in a grass–endophyte mutualism. Mol Plant Microbe Interact. 2000;13:1027–1033. https://doi.org/10.1094/MPMI.2000.13.10.1027
  • Spiering MJ, Moon CD, Wilkinson HH, Schardl CL. Gene clusters for insecticidal loline alkaloids in the grass–endophytic fungus Neotyphodium uncinatum. Genetics. 2005;169:1403–1414. https://doi.org/10.1534/genetics.104.035972
  • Huizing HJ, van der Molen W, Kloek W, Den Nijs APM. Detection of lolines in endophyte-containing meadow fescue in the Netherlands and the effect of elevated temperature on induction of lolines in endophyte-infected perennial ryegrass. Grass Forage Sci. 1999;46:441–445. https://doi.org/10.1111/j.1365-2494.1991.tb02405.x
  • Strickland JR, Bailey EM, Abney LK, Oliver JW. Assessment of the mitogenic potential of the alkaloids produced by endophyte (Acremonium coenophialum)-infected tall fescue (Festuca arundinacea) on bovine vascular smooth muscle in vitro. J Anim Sci. 1996;74:1664–1671. https://doi.org/10.2527/1996.7471664x
  • Clay K, Schardl C. Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. Am Nat. 2002;160(4 suppl):S99–S127. https://doi.org/10.1086/342161
  • Dahlman DL, Siegel MR, Bush LP. Insecticidal activity of N-formylloline. In: Proceedings of the XVIII International Grassland Congress; 1997 Jun 8–19; Winnipeg, Manitoba, Saskatoon, Saskatchewan, Canada. Calgary: International Grassland Congress; 1997. p. 13.5–13.6.
  • Riedell WE, Kieckhefer RE, Petroski RJ, Powell RG. Naturally occurring and synthetic loline alkaloid derivatives: insect feeding behavior modification and toxicity. J Entomol Sci. 1991;26:122–129. https://doi.org/10.18474/0749-8004-26.1.122
  • Johnson MC, Dahlman DL, Siegel MR, Bush LP, Latch GCM, Potter DA, et al. Insect feeding deterrents in endophyte-infected tall fescue. Applied Environmental Microbiology. 1985;49:568–571.
  • Poole DP, Littler RA, Smith BL, McLeay LM. Effects and mechanisms of action of the ergopeptides ergotamine and ergovaline and the effects of peramine on reticulum motility of sheep. Am J Vet Res. 2009;70:270–276. https://doi.org/10.2460/ajvr.70.2.270
  • Siegel, MR, Bush, LP. Defensive chemicals in grass–fungal endophyte associations. Recent Adv Phytochem. 1996;30:81–118. https://doi.org/10.1007/978-1-4899-1754-6_4
  • Schardl CL, Leuchtmann A, Spiering MJ. Symbioses of grasses with seedborne fungal endophytes. Annu Rev Plant Biol. 2004;55:315–340. https://doi.org/10.1146/annurev.arplant.55.031903.141735
  • Philippe G. Lolitrem B and indole diterpene alkaloids produced by endophytic fungi of the genus Epichloë and their toxic effects in livestock. Toxins. 2016;8:47. https://doi.org/10.3390/toxins8020047
  • Rowan DD. Lolitrems, peramine and paxilline: mycotoxins of the ryegrass/endophyte interaction. Agriculture, Ecosystems and Environment. 1993;44:103–122. https://doi.org/10.1016/0167-8809(93)90041-M
  • Di Menna ME, Finch SC, Popay AJ, Smith BL. A review of the Neotyphodium lolii / Lolium perenne symbiosis and its associated effects on animal and plant health, with particular emphasis on ryegrass staggers. N Z Vet J. 2012;60:315–328. https://doi.org/10.1080/00480169.2012.697429
  • Tapper BA, Lane GA. Janthitrems found in a Neotyphodium endophyte of perennial ryegrass. In: Kallenbach R, Rosenkrans CJ, Lock TR, editors. Proceedings of the 5th International Symposium on Neotyphodium/Grass Interactions; 2004 May 23–26; Fayetteville, AR, USA. Fayetteville, AR: University of Arkansas Press; 2004. p. 301.
  • Thom ER, Waugh CD, Minnee EMK, Waghorn GC. A new generation ryegrass endophyte – the first results from dairy cows fed AR37. In: Popay AJ, Thom ER, editors. Proceedings of the 6th International Symposium on Fungal Endophytes of Grasses; 2007 Mar 25–28; Christchurch, New Zealand. Dunedin: New Zealand Grassland Association; 2007. p. 293–296.
  • Ball OJP, Christensen MJ, Prestidge RA. Effect of selected isolates of Acremonium endophytes on adult black beetle (Heteronychus arator) feeding. N Z Plant Prot. 1994;47:227–231.
  • Popay AJ, Wyatt RT. Resistance to argentine stem weevil in perennial ryegrass infected with endophytes producing different alkaloids. N Z Plant Prot. 1995;48:229–236.
  • Popay A, Silvester WB, Gerard PJ. New endophyte isolate suppresses root aphid, Aploneura lentisci, in perennial ryegrass. In: Kallenbach R, Rosenkrans CJ, Lock TR, editors. Proceedings of the 5th International Symposium on Neotyphodium/Grass Interactions; 2004 May 23–26; Fayetteville, AR, USA. Fayetteville, AR: University of Arkansas Press; 2004. p. 317
  • Jensen JG, Popay AJ. Perennial ryegrass infected with AR37 endophyte reduces survival of porina larvae. N Z Plant Prot. 2004;57:323–328.
  • Hiroyuki K, Satoshi T, Shun-ichi T, Yoshihara T, Sakamura S, Shimanuki T, et al. New fungitoxic sesquiterpenoids, chokols A–G, from stromata of Epichloe typhina and the absolute configuration of chokol E. Agric Biol Chem. 1989;53:789–796. https://doi.org/10.1080/00021369.1989.10869341
  • Qawasmeh A, Raman A, Wheatley W, Nicol H. Antioxidative capacity of phenolic compounds extracted from Lolium perenne and Lolium arundinaceum infected with Neotyphodium (Hypocreales: Clavicipitaceae). Acta Physiol Plant. 2012;34:827–833. https://doi.org/10.1007/s11738-011-0878-6
  • Simmonds MSJ. Flavonoid-insect interactions: recent advances in our knowledge. Phytochemistry. 2003;64:21–30. https://doi.org/10.1016/S0031-9422(03)00293-0
  • Leuchtmann A. Systematics, distribution, and host specificity of grass endophytes. Nat Toxins. 1992;1:150–162. https://doi.org/10.1002/nt.2620010303
  • Belesky DP, Malinowski DP. Morphological plasticity and chemical adaptations of Neotyphodium-infected tall fescue. In: White, JF Jr, Bacon CW, editors. Microbial endophytes. New York, NY: Marcel Dekker; 2000. p. 455–484.
  • Popay AJ, Bonos SA. Biotic responses in endophytic grasses. In: Roberts CA, West CP, Spiers DE, editors. Neotyphodium in cool-season grasses. Ames, IA: Blackwell Publishing; 2005. p. 163–185. https://doi.org/10.1002/9780470384916.ch7
  • Rudgers JA, Mattingly WB, Koslow JM. Mutualistic fungus promotes plant invasion into diverse communities. Oecologia. 2005;144:463–471. https://doi.org/10.1007/s00442-005-0039-y
  • Schardl CL, Phillips TD. Protective grass endophytes: where are they from and where are they going? Plant Dis. 1997;81:430–437. https://doi.org/10.1094/PDIS.1997.81.5.430
  • Latch GCM. Physiological interactions of endophytic fungi and their hosts: biotic stress tolerance imparted to grasses by endophytes. Agriculture, Ecosystems and Environment. 1993;44:143–156. https://doi.org/10.1016/0167-8809(93)90043-O
  • Miles CO, Lane GA, di Menna ME, Garthwaite I, Piper EL, Ball OJP, et al. High levels of ergonovine and lysergic acid amide in toxic Achnatherum inebrians accompany infection by an Acremonium-like endophytic fungus. J Agric Food Chem. 1996;44:1285–1290. https://doi.org/10.1021/jf950410k
  • Miles CO, Menna ME, Jacobs SWL, Garthwaite I, Lane GA, Prestidge RA, et al. Endophytic fungi in indigenous Australasian grasses associated with toxicity to livestock. Appl Environ Microbiol. 1998;64:601–606.
  • Cabral D, Cafaro MJ, Saidman B, Lugo M, Reddy PV, White JF Jr. Evidence supporting the occurrence of a new species of endophyte in some South American grasses. Mycologia. 1999;91:315–325. https://doi.org/10.2307/3761376
  • Giuliano WM, Elliott CL, Sole JD. Significance of tall fescue in the diet of the eastern cottontail. Prairie Naturalist. 1994;26:53–60.
  • Lopez JE, Faeth SH, Miller M. Effect of endophytic fungi on herbivory by redlegged grasshoppers (Orthoptera: Acrididae) on Arizona fescue. Environ Entomol. 1995;24:1576–1580. https://doi.org/10.1093/ee/24.6.1576
  • Fortier GM, Bard N, Jansen M, Clay K. Effects of tall fescue endophyte infection and population density on growth and reproduction in prairie voles. J Wildl Manage. 2000;64:122–128. https://doi.org/10.2307/3802981
  • Conover MR, Messmer TA. Feeding preferences and changes in mass of Canada geese grazing endophyte-infected tall fescue. Condor. 1996;98:859–862. https://doi.org/10.2307/1369872
  • Madej CW, Clay K. Avian seed preference and weight loss experiments: the effect of fungal endophyte-infected tall fescue seeds. Oecologia. 1991;88:296–302. https://doi.org/10.1007/BF00320825
  • Knoch TR, Faeth SH, Arnott DL. Endophytic fungi alter foraging and dispersal by desert seed-harvesting ants. Oecologia. 1993;95:470–475. https://doi.org/10.1007/BF00317429
  • Elmi AA, West CP, Robbins RT, Kirkpatrick TL. Endophyte effects on reproduction of a root-knot nematode (Meloidogyne marylandi) and osmotic adjustment in tall fescue. Grass Forage Science. 2000;55:166–172. https://doi.org/10.1046/j.1365-2494.2000.00210.x
  • West CP, Izekor E, Oosterhuis DM, Robbins RT. The effect of Acremonium coenophialum on the growth and nematode infestation of tall fescue. Plant Soil. 1998;112:3–6. https://doi.org/10.1007/BF02181745
  • Kimmons CA, Gwinn KD, Bernard EC. Nematode reproduction on endophyte-infected and endophyte-free tall fescue. Plant Dis. 1990;74:757–761. https://doi.org/10.1094/PD-74-0757
  • Panaccione DG, Kotcon JB, Schardl CL, Johnson RD, Morton JB. Ergot alkaloids are not essential for endophytic fungus-associated population suppression of the lesion nematode, Pratylenchus scribneri, on perennial ryegrass. Nematology. 2006;8:583–590. https://doi.org/10.1163/156854106778614074
  • Rogers JK, Walker NR, Young CA. The effect of endophytic fungi on nematode populations in summer-dormant and summer-active tall fescue. J Nematol. 2016;48:87–94. https://doi.org/10.21307/jofnem-2017-013
  • Rowan DD, Hunt MB, Gaynor DL. Peramine, a novel insect feeding deterrent from ryegrass infected with the endophyte Acremonium loliae. J Chem Soc Chem Commun. 1986;142:935–936. https://doi.org/10.1039/c39860000935
  • Craven KD, Blankenship JD, Leuchtmann A, Hignight K, Schardl CL. Hybrid fungal endophytes symbiotic with the grass Lolium pratense. Sydowia. 2001;53:44–73.
  • Siegel M, Latch G, Bush L, Fannin F, Rowan D, Tapper B, et al. Fungal endophyte-infected grasses: alkaloid accumulation and aphid response. J Chem Ecol. 1990;16:3301–3315. https://doi.org/10.1007/BF00982100
  • Hartley SE, Gange AC. Impacts of plant symbiotic fungi on insect herbivores: mutualism in a multitrophic context. Annual Reviews in Entomology. 2009;54:323–342. https://doi.org/10.1146/annurev.ento.54.110807.090614
  • Lehtonen P, Helander M, Saikkonen K. Are endophyte-mediated effects on herbivores conditional on soil nutrients? Oecologia. 2005;142:38–45. https://doi.org/10.1007/s00442-004-1701-5
  • Finkes LK, Cady AB, Mulroy JC, Clay K, Rudgers JA. Plant–fungus mutualism affects spider composition in successional fields. Ecol Lett. 2006;9:347–356. https://doi.org/10.1111/j.1461-0248.2005.00882.x
  • Zabalgogeazcoa I. Review. Fungal endophytes and their interaction with plant pathogens. Spanish Journal of Agricultural Research. 2008;6:138–146. https://doi.org/10.5424/sjar/200806S1-382
  • Stovall ME, Clay K. Fungitoxic effects of Balansia cyperi (Clavicipitaceae). Mycologia. 1991;83:288–295. https://doi.org/10.1080/00275514.1991.12026012
  • Panka D, West CP, Guerber CA, Richardson MD. Susceptibility of tall fescue to Rhizoctonia zeae infection as affected by endophyte symbiosis. Ann Appl Biol. 2013;163:257–268. https://doi.org/10.1111/aab.12051
  • Ford VL, Kirkpatrick TL. Effects of Acremonium coenophialum in tall fescue on host disease and insect resistance and allelopathy to Pinus taeda seedlings. In: West CP, editor. Proceedings of the Arkansas fescue toxicosis conference. Fayetteville, AR: Arkansas Agricultural Experiment Station; 1989. p. 29–34. (Arkansas Agricultural Experiment Station Special Report; vol 140).
  • Tian P, Nan ZB, Li CJ. Effect of the endophyte Neotyphodium lolii on susceptibility and host physiological response of perennial ryegrass to fungal pathogens. Eur J Plant Pathol. 2008;122:593–602. https://doi.org/10.1007/s10658-008-9329-7
  • Clay K, Cheplick GP, Marks SM. Impact of the fungus Balansia henningsiana on the grass Panicum agrostoides: frequency of infection, plant growth and reproduction, and resistance to pests. Oecologia. 1989;80:374–380. https://doi.org/10.1007/BF00379039
  • Shimanuki T. Studies on the mechanisms of the infection of timothy with purple spot disease caused by Cladosporium phlei (Gregory) de Vries. Research Bulletin of Hokkaido National Agricultural Experiment Station. 1987;148:1–56.
  • Wang X, Qin J, Chen W, Zhou Y, Ren A, Gao Y. Pathogen resistant advantage of endophyte-infected over endophyte-free Leymus chinensis is strengthened by pre-drought treatment. Eur J Plant Pathol. 2016;144:477–486. https://doi.org/10.1007/s10658-015-0788-3
  • Welty RE, Barker RE, Azevedo MD. Reaction of tall fescue infected and noninfected by Acremonium coenophialum to Puccinia graminis subsp. graminicola. Plant Dis. 1991;75:883–886. https://doi.org/10.1094/PD-75-0883
  • Rochow WF, Duffus JE. Luteoviruses and yellows diseases. In: Kurstak E, editor. Handbook of plant virus infections and comparative diagnosis. Amsterdam: Elsevier; 1981. p. 147–170.
  • Mahmood T, Gergerich RC, Milus EA, West CP, D’Arcy CJ. Barley yellow dwarf viruses in wheat, endophyte-infected and endophyte-free tall fescue, and other hosts in Arkansas. Plant Dis. 1993;77:225–228. https://doi.org/10.1094/PD-77-0225
  • Lehtonen PT, Helander M, Siddiqui SA, Lehto K, Saikkonen K. Endophytic fungus decreases plant virus infections in meadow ryegrass (Lolium pratense). Biol Lett. 2006;2:620–623. https://doi.org/10.1098/rsbl.2006.0499
  • Romo M, Leuchtmann A, García B, Zabalgogeazcoa I. A totivirus infecting the mutualistic fungal endophyte Epichloë festucae. Virus Res. 2007;124:38–43. https://doi.org/10.1016/j.virusres.2006.09.008
  • Herrero N, Sánchez S, Zabalgogeazcoa I. Mycoviruses are common among different species of fungal endophytes of grasses. Arch Virol. 2009;154:327–330. https://doi.org/10.1007/s00705-008-0293-5
  • Smith SE, Gianinazzi-Pearson V. Physiological interactions between symbionts in vesicular-arbuscular mycorrhizal plants. Annual Reviews of Plant Physiology and Plant Molecular Biology. 1988;39:221–244. https://doi.org/10.1146/annurev.pp.39.060188.001253
  • Vignale MV, Iannone LJ, Scervino JM, Novas MV. Epichloë exudates promote in vitro and in vivo arbuscular mycorrhizal fungi development and plant growth. Plant Soil. 2018;422:267–281. https://doi.org/10.1007/s11104-017-3173-5
  • Chu-Chou M, Guo B, An ZQ, Hendrix JW, Ferris RS, Siegel MR, et al. Suppression of mycorrhizal fungi in fescue by the Acremonium coenophialum endophyte. Soil Biology and Biochemistry. 1992;24:633–637. https://doi.org/10.1016/0038-0717(92)90041-U
  • Müller J. Artificial infection by endophytes affect growth and mycorrhizal colonisation of Lolium perenne. Funct Plant Biol. 2003;30:419–424. https://doi.org/10.1071/FP02189
  • Omacini M, Eggers T, Bonkowski M, Gange AC, Jones TH. Leaf endophytes affect mycorrhizal status of co-infected and neighbouring plant. Funct Ecol. 2006;20:226–232. https://doi.org/10.1111/j.1365-2435.2006.01099.x
  • Mack KML, Rudgers JA. Balancing multiple mutualists: asymmetric interactions among plants, arbuscular mycorrhizal fungi, and fungal endophytes. Oikos. 2008;117:310–320. https://doi.org/10.1111/j.2007.0030-1299.15973.x
  • Novas MV, Cabral D, Godeas AM. Interaction between grass endophytes and mycorrhizas in Bromus setifolius from Patagonia, Argentina. Symbiosis. 2005;40:23–30.
  • Novas MV, Iannone LJ, Godeas A, Cabral D. Positive association between mycorrhiza and foliar endophytes in Poa bonariensis, a native grass. Mycol Prog. 2009;8:75–81. https://doi.org/10.1007/s11557-008-0579-8
  • Cheplick GP, Faeth SH. Ecology and evolution of the grass–endophyte symbiosis. New York, NY: Oxford University Press, Inc.; 2009. https://doi.org/10.1093/acprof:oso/9780195308082.001.0001
  • Barker GM. Mycorrhizal infection influences Acremonium-induced resistance to argentine stem weevil in ryegrass. In: Popay AJ, editor. Proceedings of the 40th N. Z. Weed and Pest Control Conference; 1987 Aug 11–13; Nelson, New Zealand. Nelson: The New Zealand Weed and Pest Control Society Inc.; 1987. p. 199–203.
  • Vicari M, Hatcher PE, Ayres PG. Combined effect of foliar and mycorrhizal endophytes on an insect herbivore. Ecology. 2002;83:2452–2464. https://doi.org/10.1890/0012-9658(2002)083[2452:CEOFAM]2.0.CO;2
  • Asao T, Hasegawa K, Sueda Y, Tomita K, Taniguchi K, Hosoki T, et al. Autotoxicity of root exudates from taro. Scienta Horticulturae. 2003;97:389–396. https://doi.org/10.1016/S0304-4238(02)00197-8
  • Kalinova J, Vrchotova N, Triska J. Exudation of allelopathic substances in buckwheat (Fagopyrum esculentum Moench). Journal of Agriculture and Food Chemistry. 2007;55:6453–6459. https://doi.org/10.1021/jf070795u
  • Guo J, McCulley RL, McNear DH Jr. Tall fescue cultivar and fungal endophyte combinations influence plant growth and root exudate composition. Front Plant Sci. 2015;6:183. https://doi.org/10.3389/fpls.2015.00183
  • Yu JQ, Matsui Y. Phytotoxic substances in root exudates of cucumber (Cucumis sativus L.). J Chem Ecol. 1994;20:21–31. https://doi.org/10.1007/BF02065988
  • Al-Sherif E, Hegazy AK, Gomaa NH, Hassan MO. Allelopathic effect of black mustard tissues and root exudates on some crops and weeds. Planta Daninha. 2013;31:11–19. https://doi.org/10.1590/S0100-83582013000100002
  • Renne IJ, Rios BG, Fehmi JS, Tracy BF. Low allelopathic potential of an invasive forage grass on native grassland plants: a cause for encouragement? Basic Appl Ecol. 2004;5:261–269. https://doi.org/10.1016/j.baae.2003.11.001
  • van Hecke MM, Treonis AM, Kaufman JR. How does the fungal endophyte Neotyphodium coenophialum affect tall fescue (Festuca arundinacea) rhizodeposition and soil microorganisms? Plan Soil. 2005;275:101–109. https://doi.org/10.1007/s11104-005-0380-2
  • Arraudeau MA. Breeding strategies for drought resistance. In: Baker FWC, editor. Drought resistance in cereals. Wallingford: CAB International; 1989. p. 107–116.
  • Latch GCM, Hunt WF, Musgrave DR. Endophytic fungi affect growth of perennial ryegrass. New Zealand Journal of Agricultural Research. 1985;28:165–168. https://doi.org/10.1080/00288233.1985.10427011
  • de Battista JP, Bouton JH, Bacon CW, Siegel MR. Rhizome and herbage production of endophyte removed tall fescue clones and populations. Agron J. 1990;82:651–654.
  • Marks S, Clay K, Cheplick GP. Effects of fungal endophytes on interspecific and intraspecific competition in the grasses Festuca arundinacea and Lolium perenne. J Appl Ecol. 1991;28:194–204. https://doi.org/10.2307/2404125
  • Malinowski D, Leuchtmann A, Schmidt D, Nösberger J. Symbiosis with Neotyphodium uncinatum endophyte may increase the competitive ability of meadow fescue. Agron J. 1997;89:833–839. https://doi.org/10.2134/agronj1997.00021962008900050019x
  • Elmi AA, West CP. Endophyte infection effects on stomatal conductance, osmotic adjustment and drought recovery of tall fescue. New Phytol. 1995;131:61–67. https://doi.org/10.1111/j.1469-8137.1995.tb03055.x
  • Buck GW, West CP, Elbersen HW. Endophyte effect on drought tolerance in diverse Festuca species. In: Bacon CW, Hill NS, editors. Neotyphodium/grass interactions. New York, NY: Plenum Press; 1997. p. 141–143. https://doi.org/10.1007/978-1-4899-0271-9_21
  • Elbersen HW, West CP. Growth and water relations of field-grown tall fescue as influenced by drought and endophyte. Grass Forage Sci. 1996;51:333–342. https://doi.org/10.1111/j.1365-2494.1996.tb02068.x
  • Richardson MD, Chapman GW Jr, Hoveland CS, Bacon CW. Sugar alkohols in endophyte-infected tall fescue. Crop Sci. 1992;32:1060–1061. https://doi.org/10.2135/cropsci1992.0011183X003200040045x
  • Bayat F, Mirlohi A, Khodambashi M. Effects of endophytic fungi on some drought tolerance mechanisms of tall fescue in a hydroponics culture. Russ J Plant Physiol. 2009;56:510–516. https://doi.org/10.1134/S1021443709040104
  • Nagabhyru P, Dinkins RD, Wood CL, Bacon CW, Schardl CL. Tall fescue endophyte effects on tolerance to water-deficit stress. BMC Plant Biol. 2013;13:127. https://doi.org/1471-2229/13/127
  • Barker DJ, Sullivan CY, Moser LE. Water deficit effects on osmotic potential, cell wall elasticity and proline in five forage grasses. Agron J. 1993;85:270–275. https://doi.org/10.2134/agronj1993.00021962008500020020x
  • Abernethy GA, McManus MT. Biochemical responses to an imposed water deficit in mature leaf tissue of Festuca arundinacea. Environmental Experimental Botany. 1998;40:17–28. https://doi.org/10.1016/S0098-8472(98)00017-3
  • White RH, Engelke MC, Morton SJ, Johnson-Cicalese JM, Ruemmele BA. Acremonium endophyte effects on tall fescue drought tolerance. Crop Sci. 1992;32:1392–1396. https://doi.org/10.2135/cropsci1992.0011183X003200060017x
  • Malinowski D. Rhizomatous ecotypes and symbiosis with endophytes as new possibilities of improvement in competitive ability of meadow fescue (Festuca pratensis Huds.) [PhD thesis]. Zurich: Swiss Federal Institute of Technology; 1995. https://doi.org/10.3929/ethz-a-001575829
  • Johnson RC, Tieszen LL. Carbon isotope discrimination, water relations, and gas exchange in temperate grass species and accessions. In: Ehleringer JR, Hall AE, Farquhar GD, editors. Stable isotopes and plant carbon–water relations. San Diego, CA: Academic Press, Inc; 1993. p. 281–296. https://doi.org/10.1016/B978-0-08-091801-3.50027-1
  • Eerens JPJ, Lucas RJ, Easton HS, White JGH. Influence of the endophyte (Neotyphodium lolii ) on morphology, physiology, and alkaloid synthesis of perennial ryegrass during high temperature and water stress. New Zealand Journal of Agricultural Research. 1998;41:219–226. https://doi.org/10.1080/00288233.1998.9513305
  • West CP, Carson RD, Guerber CA, de los Reyes B. Endophyte effects on antioxidants and membrane leakage in tall fescue during drought. In: Proceedings of the 4th International Symposium on the Molecular Breeding of Forage and Turf, a satellite workshop of the XXth International Grassland Congress; 2005 Jul; Aberystwyth, Wales; Wageningen: Wageningen Academic Publishers; 2005. p. 217–218.
  • Zhang YP, Nan ZB. Growth and anti-oxidative systems changes in Elymus dahuricus is affected by Neotyphodium endophyte under contrasting water availability. J Agron Crop Sci. 2007;193:377–386. https://doi.org/10.1111/j.1439-037X.2007.00279.x
  • Torres MS, White JF Jr, Zhang X, Hinton DM, Bacon CW. Endophyte-mediated adjustments in host morphology and physiology and effects on host fitness traits in grasses. Fungal Ecol. 2012;5:322–330. https://doi.org/10.1016/j.funeco.2011.05.006
  • West CP, Elbersen HW, Elmi AA, Buck GW. Acremonium effects on tall fescue growth: parasite or stimulant? In: Brink GE, editor. Proceedings of the 50th Southern Pasture Forage Crop Improvement Conference; 1994 May 23–25; Knoxville, TN, USA. Knoxville, TN: [publisher unknown]; 1994. p. 102–111.
  • Volaire F. Drought survival, summer dormancy and dehydrin accumulation in contrasting cultivars of Dactylis glomerata. Physiol Plant. 2002;116:42–51. https://doi.org/10.1034/j.1399-3054.2002.1160106.x
  • Allagulova CR, Gimalov FR, Shakirova FM, Vakhitov VA. The plant dehydrins: structure and putative functions. Biochemistry (Moscow). 2003;68:945–951. https://doi.org/10.1023/A:1026077825584
  • Koag MC, Fenton RD, Wilkens S, Close TJ. The binding of maize DHN1 to lipid vesicles. Gain of structure and lipid specificity. Plant Physiol. 2003;131:309–316. https://doi.org/10.1104/pp.011171
  • Carson RD. Biochemical responses of tall fescue to endophyte infection during water deficit [Master thesis]. Fayetteville: University of Arkansas Library; 2004.
  • Guerber CA, West CP, Carson RD, Havely AM. Dehydrin expression in drought-stressed tall fescue. In: Popay AJ, Thom ER, editors. Proceedings of the 6th International Symposium on Endophyte–Grass Interactions; 2006 Mar 26–28; Christchurch, New Zealand. Christchurch: New Zealand Grassland Association; 2007. p. 225–227. (Grassland Research and Practice Series; vol 13).
  • Jiang Y, Huang B. Protein alterations in tall fescue in response to drought stress and abscisic acid. Crop Sci. 2002;42:202–207. https://doi.org/10.2135/cropsci2002.2020
  • Carrow RN. Drought avoidance characteristics of diverse tall fescue cultivars. Crop Sci. 1996;36:371–377. https://doi.org/10.2135/cropsci1996.0011183X003600020026x
  • Crush JR, Popay AJ, Waller J. Effect of different Neotyphodium endophytes on root distribution of a perennial ryegrass (Lolium perenne L.) cultivar. New Zealand Journal of Agricultural Research. 2004;47:345–349. https://doi.org/10.1080/00288233.2004.9513603
  • Ding N, Kupper JV, McNear DH Jr. Phosphate source interacts with endophyte strain to influence biomass and root system architecture in tall fescue. Agron J. 2015;107:662–670. https://doi.org/10.2134/agronj14.0135
  • Malinowski DP, Belesky DP. Neotyphodium coenophialum endophyte infection affects the ability of tall fescue to use sparingly available phosphorus. J Plant Nutr. 1999;22:835–853. https://doi.org/10.1080/01904169909365675
  • Malinowski DP, Zuo H, Belesky DP, Alloush GA. Evidence for copper binding by extracellular root exudates of tall fescue but not perennial ryegrass infected with Neotyphodium spp. endophytes. Plant Soil. 2004;267:1–12. https://doi.org/10.1007/s11104-005-2575-y
  • Belesky DP, Stuedemann JA, Plattner RD, Wilkinson SR. Ergopeptine alkaloids in grazed tall fescue. Agron J. 1988;80:209–212. https://doi.org/10.2134/agronj1988.00021962008000020014x
  • Lyons PC, Evans JJ, Bacon CW. Effects of the fungal endophyte Acremonium coenophialum on nitrogen accumulation and metabolism in tall fescue. Plant Physiol. 1990;92:726–732. https://doi.org/10.1104/pp.92.3.726
  • Belesky DP, Wilkinson SR, Pallas JE Jr. Response of four tall fescue cultivars grown at two nitrogen levels to low soil water availability. Crop Sci. 1982;22:93–97. https://doi.org/10.2135/cropsci1982.0011183X002200010021x
  • Belesky DP, Wilkinson SR, Evans JJ. Amino acid composition of fractions of ‘Kentucky-31’ tall fescue as affected by N fertilization and mild water stress. Plant Soil. 1984;81:257–267. https://doi.org/10.1007/BF02197159
  • Malinowski DP, Alloush GA, Belesky DP. Evidence for chemical changes on the root surface of tall fescue in response to infection with the fungal endophyte Neotyphodium coenophialum. Plant Soil. 1998;205:1–12. https://doi.org/10.1023/A:1004331932018
  • Malinowski DP, Belesky DP. Tall fescue aluminum tolerance is affected by Neotyphodium coenophialum endophyte. J Plant Nutr. 1999;22:1335–1349. https://doi.org/10.1080/01904169909365716
  • Malinowski DP, Alloush GA, Belesky DP. Leaf endophyte Neotyphodium coenophialum modifies mineral uptake in tall fescue. Plant Soil. 2000;227:115–126. https://doi.org/10.1023/A:1026518828237
  • Ren AZ, Gao YB, Zhou F. Response of Neotyphodium lolii-infected perennial ryegrass to phosphorus deficiency. Plant Soil Environ. 2007;53:113–119. https://doi.org/10.17221/2225-PSE
  • Appel HM. Phenolics in ecological interactions: the importance of oxidation. J Chem Ecol. 1993;19:1521–1552. https://doi.org/10.1007/BF00984895
  • Kafkafi U, Bar-Yosef B, Rosenberg R, Sposito G. Phosphorus adsorption by kaoloinite and montmorillonite: II. Organic anion competition. Soil Sci Soc Am J. 1988;52:1585–1589. https://doi.org/10.2136/sssaj1988.03615995005200060012x
  • Rahman MH, Saiga S. Endophyte effects on nutrient acquisition in tall fescue grown in andisols. J Plant Nutr. 2007;30:2141–2158. https://doi.org/10.1080/01904160701700632
  • Dennis SB, Allen VG, Saker KE, Fontenot JP, Ayad JY, Brown CP. Influence of Neotyphodium coenophialum on copper concentration in tall fescue. J Anim Sci. 1998;76:2687–2693. https://doi.org/10.2527/1998.76102687x
  • Marschner, H. Mineral nutrition in higher plants. 2nd ed. Orlando, FL: Academic Press; 1995. https://doi.org/10.1016/B978-012473542-2/50008-0
  • van Hecke MM, Treonis AM, Kaufman JR. How does the fungal endophyte Neotyphodium coenophialum affect tall fescue (Festuca arundinacea) rhizodeposition and soil microorganisms? Plant Soil. 2005;275:101–109. https://doi.org/10.1007/s11104-005-0380-2
  • Fabien M, Nathalle V, Adnan H, Alain C, Huguette S. Endophytic Neotyphodium lolii induced tolerance to Zn stress in Lolium perenne. Plant Physiol. 2001;113:557–563. https://doi.org/10.1034/j.1399-3054.2001.1130415.x
  • Zamani N, Sabzalian MR, Khoshgoftarmanesh A, Afyuni M. Neotyphodium endophyte changes phytoextraction of zinc in Festuca arundinacea and Lolium perenne. Int J Phytoremediation. 2014;17:456–463. https://doi.org/10.1080/15226514.2014.922919
  • Zaurov DE, Bonos S, Murphy JA, Richardson M, Belanger F. Endophyte infection can contribute to aluminum tolerance in fine fescues. Crop Sci. 2001;41:1981–1984. https://doi.org/10.2135/cropsci2001.1981
  • Soleimani M, Hajabbasi MA, Afyuni M, Mirlohi A, Borggaard OK, Holm PE. Effect of endophytic fungi on cadmium tolerance and bioaccumulation by Festuca arundinacea and Festuca pratensis. Int J Phytoremediation. 2010;12:535–549. https://doi.org/10.1080/15226510903353187
  • Zhang X, Fan X, Li C, Nan Z. Effects of cadmium stress on seed germination, seedling growth and antioxidative enzymes in Achnatherum inebrians plants infected with a Neotyphodium endophyte. Plant Growth Regul. 2010;60:91–97. https://doi.org/10.1007/s10725-009-9422-8
  • Mirzahosseini Z, Shabani L, Sabzalian MR, Sharifi Tehrani M. Effect of Neotyphodium endophyte symbiosis on growth, nickel uptake and photosynthetic pigments in two genotypes of tall fescue. Journal of Plant Processes and Function. 2014;2:25–37.
  • Bonnet M, Camares O, Veisseire P. Effects of zinc and influence of Acremonium lolii on growth parameters, chlorophyll a fluorescence and antioxidant enzyme activities of ryegrass (Lolium perenne L. cv Apollo). J Exp Bot. 2000;51:945–953. https://doi.org/10.1093/jexbot/51.346.945
  • Yin L, Ren A, Wei M, Wu L, Zhou Y, Li X, Gao Y. Neotyphodium coenophialum-infected tall fescue and its potential application in the phytoremediation of saline soils. Int J Phytoremediation. 2014;16:235–246. https://doi.org/10.1080/15226514.2013.773275
  • Belesky DP, Devine OJ, Pallas JE, Stringer WC. Photosynthetic activity of tall fescue as influenced by a fungal endophyte. Photosynthetica. 1987;21:82–87.
  • Lewis GC. Effects of biotic and abiotic stress on the growth of three genotypes of Lolium perenne with and without infection by the fungal endophyte Neotyphodium lolii. Ann Appl Biol. 2004;144:53–63. https://doi.org/10.1111/j.1744-7348.2004.tb00316.x
  • Davitt AJ, Stansberry M, Rudgers JA. Do the costs and benefits of fungal endophyte symbiosis vary with light availability? New Phytol. 2010;188:824–834. https://doi.org/10.1111/j.1469-8137.2010.03428.x
  • Newsham KK, Lewis GC, Greensdale PD, McLeod AR. Neotyphodium lolii, a fungal leaf endophyte, reduces fertility of Lolium perenne exposed to elevated UV-B radiation. Ann Bot. 1998;81:397–403. https://doi.org/10.1006/anbo.1997.0572
  • McLeod AR, Rey A, Newsham KK, Lewis GC, Wolferstan P. Effects of elevated ultraviolet radiation and endophytic fungi on plant growth and insect feeding in Lolium perenne, Festuca rubra, F. arundinacea and F. pratensis. Journal of Photochemistry and Photobiology. 2001;B62:97–107. https://doi.org/10.1016/S1011-1344(01)00151-8
  • Zhou F, Gao Y, Ma W. Effects of phosphorus deficiency on growth of perennial ryegrass–fungal endophyte symbiont and phenolic content in root. Plant Physiology Communications. 2003;39:321–324.
  • Blokhina O, Virolainen E, Fagerstedt KV. Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann Bot. 2003;91:179–194. https://doi.org/10.1093/aob/mcf118
  • Malinowski DP, Belesky DP, Lewis GC. Abiotic stresses in endophytic grasses. In: Roberts CA. West CP, Spiers DE, editors. Neotyphodium in cool season grasses. Ames, IA: Blackwell Publishing Professional; 2005. p. 187–199. https://doi.org/10.1002/9780470384916.ch8
  • Belesky DP, Bacon CW. Tall fescue and associated mutualistic toxic fungal endophytes in agroecosystems. Toxin Rev. 2009;28:102–117. https://doi.org/10.1080/15569540903082143
  • Spyreas G, Gibson DJ, Middleton BA. Effects of endophyte infection in tall fescue (Festuca arundinacea: Poaceae) on community diversity. Int J Plant Sci. 2001;162:1237–1245. https://doi.org/10.1086/323274
  • Gundel PE, Garibaldi LA, Martínez‐Ghersa MA, Ghersa CM. Neotyphodium endophyte transmission to Lolium multiflorum seeds depends on the host plant fitness. Environ Exp Bot. 2011;71:359–366. https://doi.org/10.1016/j.envexpbot.2011.02.002
  • Iqbal J, Nelson JA, McCulley RL. Fungal endophyte presence and genotype affect plant diversity and soil-to-atmosphere trace gas fluxes. Plant Soil. 2013;364:15–27. https://doi.org/10.1007/s11104-012-1326-0
  • Franzluebbers AJ, Nazih N, Stuedemann JA, Fuhrmann JJ, Schomberg HH, Hartel PG. Soil carbon and nitrogen pools under low- and high-endophyte-infected tall fescue. Soil Sci Soc Am J. 1999;63:1687–1694. https://doi.org/10.2136/sssaj1999.6361687x
  • Omacini M, Chaneton EJ, Ghersa CM, Otero P. Do foliar endophytes affect grass litter decomposition? A microcosm approach using Lolium multiflorum. Oikos. 2004;104:581–590. https://doi.org/10.1111/j.0030-1299.2004.12915.x
  • Lemons A, Clay K, Rudgers JA. Connecting plant–microbial interactions above and belowground: a fungal endophyte affects decomposition. Oecologia. 2005;145:595–604. https://doi.org/10.1007/s00442-005-0163-8
  • Petroski RJ, Dornbos DL Jr, Powell RG. Germination and growth inhibition of annual ryegrass (Lolium multiflorum L.) and alfalfa (Medicago sativa L.) by loline alkaloids and synthetic N-acylloline derivatives. Journal of Agriculture and Food Chemistry. 1990;38:1716–1718. https://doi.org/10.1021/jf00098a019
  • Malinowski DP, Belesky DP, Fedders JM. Endophyte infection may affect the competitive ability of tall fescue grown with red clover. J Agron Crop Sci. 1999;183:91–101. https://doi.org/10.1046/j.1439-037x.1999.00322.x
  • Sutherland BL, Hume DE, Tapper BA. Allelopathic effects of endophyte-infected perennial ryegrass extracts on white clover seedlings. New Zealand Journal of Agricultural Research. 1999;42:19–26. https://doi.org/10.1080/00288233.1999.9513349
  • Matthews JW, Clay K. Influence of fungal endophyte infection on plant–soil feedback and community interactions. Ecology. 2001;82:500–509. https://doi.org/10.1890/0012-9658(2001)082[0500:IOFEIO]2.0.CO;2
  • Buyer JS, Zuberer DA, Nichols KA, Franzluebbers AJ. Soil microbial community function, structure, and glomalin in response to tall fescue endophyte infection. Plant Soil. 2011;339:401–412. https://doi.org/10.1007/s11104-010-0592-y
  • Casas C, Omacini M, Susana Montecchia M, Susana Correa O. Soil microbial community responses to the fungal endophyte Neotyphodium in Italian ryegrass. Plant Soil. 2011;340:347–355. https://doi.org/10.1007/s11104-010-0607-8
  • Hoveland CS, Bouton JH, Durham RG. Fungal endophyte effects on production of legumes in association with tall fescue. Agron J. 1999;91:897–902. https://doi.org/10.2134/agronj1999.916897x
  • Takai T, Sanada Y, Yamada T. Influence of the fungal endophyte Neotyphodium uncinatum on the persistency and competitive ability of meadow fescue (Festuca pratensis Huds.). Japanese Society of Grassland Science. 2010;56:59–64. https://doi.org/10.1111/j.1744-697X.2010.00175.x
  • Rudgers JA, Fischer, S, Clay K. Managing plant symbiosis: fungal endophyte genotype alters plant community composition. J Appl Ecol. 2010;47:468–477. https://doi.org/10.1111/j.1365-2664.2010.01788.x
  • Yurkonis KA, Shukla K, Holdenried J, Hager HA, Bolton KA, Klironomos JN, et al. Endophytes inconsistently affect plant communities across Schedonorus arundinaceus hosts. Plant Ecol. 2014;215:389–398. https://doi.org/10.1007/s11258-014-0309-z
  • Marks S, Clay K. Effects of CO2 enrichment, nutrient addition, and fungal endophyte-infection on the growth of two grasses. Oecologia. 1990;84:207–214. https://doi.org/10.1007/BF00318273
  • Briggs L, Crush J, Ouyang L, Sprosen J. Neotyphodium endophyte strain and superoxide dismutase activity in perennial ryegrass plants under water deficit. Acta Physiol Plant. 2013;35:1513–1520. https://doi.org/10.1007/s11738-012-1192-7
  • Ambrose KV, Tian Z, Wang Y, Smith J, Zylstra G, Huang B, et al. Functional characterization of salicylate hydroxylase from the fungal endophyte Epichloë festucae. Sci Rep. 2015;5:10939. https://doi.org/10.1038/srep10939
  • Bastías DA, Alejandra Martínez-Ghersa M, Newman JA, Card SD, Mace WJ, Gundel PE. The plant hormone salicylic acid interacts with the mechanism of anti-herbivory conferred by fungal endophytes in grasses. Plant Cell Environ. 2018;41:395–405. https://doi.org/10.1111/pce.13102
  • Clay K. Effects of fungal endophytes on the seed and seedling biology of Lolium perenne and Festuca arundinacea. Oecologia. 1987;73:358–362. https://doi.org/10.1007/BF00385251
  • Pinkerton BW, Rice JS, Undersander DJ. Germination in Festuca arundinacea as affected by the fungal endophyte, Acremonium coenophialum. In: Quinsenberry SS, Joost RE, editors. Proceedings of the International Symposium on Acremonium/Grass Interactions; 1990 Nov 3; Baton Rouge, LA, USA. Baton Rouge, LA: Louisiana Agricultural Experiment Station; 1990. p. 176–180.
  • Novas MV, Gentile A, Cabral D. Comparative study of growth parameters on diaspores and seedlings between populations of Bromus setifolius from Patagonia, differing in Neotyphodium endophyte infection. Flora. 2003;198:421–426. https://doi.org/10.1078/0367-2530-00115
  • Li CJ, Nan ZB, Li F. Biological and physiological characteristics of Neotyphodium gansuense symbiotic with Achnatherum inebrians. Microbiol Res. 2008;163:431–440. https://doi.org/10.1016/j.micres.2006.07.007
  • Wang J, Zhou Y, Lin W, Li M, Wang M, Wang Z, et al. Effect of an Epichloë endophyte on adaptability to water stress in Festuca sinensis. Fungal Ecol. 2017;30:39–47. https://doi.org/10.1016/j.funeco.2017.08.005
  • Faeth SH, Helander ML, Saikkonen KT. Asexual Neotyphodium endophytes in a native grass reduce competitive abilities. Ecol Lett. 2004;7:304–313. https://doi.org/10.1111/j.1461-0248.2004.00578.x
  • Owens HT, Finneseth CH, Tillery TM, Phillips TD. Germination rate and seedling vigour of tall fescue as affected by endophyte status and seed density. In: Popay AJ, Thom ER, editors. Proceedings of the 6th International Symposium on Fungal Endophytes of Grasses; 2007 Mar 25–28; Christchurch, New Zealand. Dunedin: New Zealand Grassland Association; 2007. p. 271–274.
  • Wäli PR, Helander M, Saloniemi I, Ahlholm J, Saikkonen K. Variable effects of endophytic fungus on seedling establishment of fine fescues. Oecologia. 2009;159:49–57. https://doi.org/10.1007/s00442-008-1202-z
  • Hill NS, Stringer WC, Rottinghaus GE, Belesky DP, Parrot WA, Pope DD. Growth, morphological and chemical component responses of tall fescue to Acremonium coenophialum. Crop Sci. 1990;30:156–161. https://doi.org/10.2135/cropsci1990.0011183X003000010034x
  • Eerens JPJ, White JGH, Lucas RJ. The influence of Acremonium endophyte on the leaf extension rate of moisture stressed ryegrass plants. In: Hume DE et al., editors. Proceedings of the 2nd International Symposium on Acremonium/Grass Interactions; 1993 Feb 4–6; Palmerston North, New Zealand. Palmerston North: AgResearch, Grassland Research Centre; 1993. p. 200–204.
  • Malinowski DP, Brauer DK, Belesky DP. The endophyte Neotyphodium coenophialum affects root morphology of tall fescue grown under phosphorus deficiency. J Agron Crop Sci. 1999;183:53–60. https://doi.org/10.1046/j.1439-037x.1999.00321.x
  • Vázquez-de-Aldana BR, Zabalgogeazcoa I, García-Ciudad A, García-Criado B. An Epichloë endophyte affects the competitive ability of Festuca rubra against other grassland species. Plant Soil. 2013;362:201–213. https://doi.org/10.1007/s11104-012-1283-7
  • Chen W, Liu H, Wurihan, Gao Y, Card SD, Ren A. The advantages of endophyte-infected over uninfected tall fescue in the growth and pathogen resistance are counteracted by elevated CO2. Sci Rep. 2017;7:6952. https://doi.org/10.1038/s41598-017-07183-y
  • Stocker TF, Qin D, Plattner GK, Tignor M, Allen SK, Boschung J, et al, editors. Climate Change 2013: the physical science basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge: Cambridge University Press; 2013.
  • Hunt MG, Rasmussen SPCD, Parsons AJ, Newman JA. Near-term impacts of elevated CO2, nitrogen and fungal endophyte-infection on Lolium perenne L. growth, chemical composition and alkaloid production. Plant Cell Environ. 2005;28:1345–1354. https://doi.org/10.1111/j.1365-3040.2005.01367.x
  • Newman JA, Abner ML, Dado RG, Gibson DJ, Brookings A, Parson AJ. Effects of elevated CO2, nitrogen and fungal endophyte-infection on tall fescue: growth, photosynthesis, chemical composition and digestibility. Glob Chang Biol. 2003;9:425–437. https://doi.org/10.1046/j.1365-2486.2003.00601.x
  • Volaire F, Norton M. Summer dormancy in perennial temperate grasses. Ann Bot. 2006;98:927–933. https://doi.org/10.1093/aob/mcl195
  • Clement SL, Elberson LR, Youssef NN, Davitt CM, Doss RP. Incidence and diversity of Neotyphodium fungal endophytes in tall fescue from Morocco, Tunisia, and Sardinia. Crop Sci. 2001;41:570–576. https://doi.org/10.2135/cropsci2001.412570x
  • Piano E, Bertoli FB, Romani M. Specificity of host-endophyte association in tall fescue populations from Sardinia, Italy. Crop Sci. 2005;45:1456–1463. https://doi.org/10.2135/cropsci2004.0287
  • Pecetti L, Romani M, Carroni AM, Annicchiarico P, Piano E. The effect of endophyte infection on persistence of tall fescue (Festuca arundinacea Schreb.) populations in two climatically contrasting Italian locations. Aust J Agric Res. 2007;58:893–899. https://doi.org/10.1071/AR06423
  • Pecetti L, Annicchiarico P, Porqueddu C, Khedim A, Abdelguerfi A. Fitting germplasm types of tall fescue and orchardgrass to different cropping environments of the Mediterranean region. Crop Sci. 2009;49:2393–2399. https://doi.org/10.2135/cropsci2009.06.0333
  • Malinowski DP, Butler TJ, Belesky DP. Competitive ability of tall fescue against alfalfa as a function of summer dormancy, endophyte infection, and soil moisture availability. Crop Sci. 2011;51:1282–1290. https://doi.org/10.2135/cropsci2010.08.0456
  • Brem D, Leuchtmann A. Intraspecific competition of endophyte infected vs uninfected plants of two woodland grass species. Oikos. 2002;96:281–290. https://doi.org/10.1034/j.1600-0706.2002.960210.x
  • Saikkonen K, Lehtonen P, Helander M, Koricheva J, Faeth SH. Model systems in ecology: dissecting the endophyte-grass literature. Trends Plant Sci. 2006;11:428–433. https://doi.org/10.1016/j.tplants.2006.07.001
  • Tapper BA, Latch GCM. Selection against toxin production in endophyte-infected perennial ryegrass. In: Woodfield DR, Matthew C, editors. Ryegrass endophyte: an essential New Zealand symbiosis. Palmerston North: New Zealand Grassland Association; 1999. p. 107–111. (Grassland Research and Practice Series; vol 7).
  • Bouton JH, Latch GCM, Hill NS, Hoveland CS, McCann MA, Watson RH, et al. Reinfection of tall fescue cultivars with non-ergot alkaloid-producing endophytes. Agron J. 2002;94:567–574. https://doi.org/10.2134/agronj2002.5670
  • Parish JA, McCann MA, Watson RH, Hoveland CS, Hawkins LL, Hill NS, et al. Use of nonergot alkaloid-producing endophytes for alleviating tall fescue toxicosis in sheep. J Anim Sci. 2003;81:1316–1322. https://doi.org/10.2527/2003.8151316x
  • Parish JA, McCann MA, Watson RH, Paiva NN, Hoveland CS, Parks AH, et al. Use of nonergot alkaloid-producing endophytes for alleviating tall fescue toxicosis in stocker cattle. J Anim Sci. 2003;81:2856–2868. https://doi.org/10.2527/2003.81112856x
  • Nihsen ME, Piper EL, West CP, Crawford RJ Jr, Denard TM, Johnson ZB, et al. Growth rate and physiology of steers grazing tall fescue inoculated with novel endophytes. J Anim Sci. 2004;82:878–883. https://doi.org/10.1093/ansci/82.3.878
  • Gunter SA, Beck PA. Novel endophyte-infected tall fescue for growing beef cattle. J Anim Sci. 2004;82:E75–E82.
  • Hopkins AA, Young CA, Panaccione DG, Simpson WR, Mittal S, Bouton JH. Agronomic performance and lamb health among several tall fescue novel endophyte combinations in the South-Central USA. Crop Sci. 2009;50:1552–1561. https://doi.org/10.2135/cropsci2009.08.0473
  • Gundel PE, Pérez LI, Helander M, Saikkonen K. Symbiotically modified organisms: nontoxic fungal endophytes in grasses. Trends Plant Sci. 2013;18:420–427. https://doi.org/10.1016/j.tplants.2013.03.003
  • Macoon B, Vann RC, Perkins JD III, Withers FT Jr. Steer performance and forage production on novel-endophyte fescue compared to ryegrass pastures. In: Kallenbach R, Rosenkrans C Jr, Lock TR, editors. Proceedings of the 5th International Symposium on Neotyphodium/Grass Interactions; 2004 May 23–26; Fayetteville, AR, USA. Fayetteville, AR: University of Arkansas; 2004. Poster No. 504.
  • Hopkins AA, Young CA, Butler TJ, Bouton JH. Registration of ‘Texoma’ MaxQ II tall fescue. J Plant Regist. 2011;5:14–18. https://doi.org/10.3198/jpr2010.02.0082crc
  • New Zealand Agriseeds. Endophyte options [Internet]. 2018 [cited 2018 Sep 27]. Available from: https://www.agriseeds.co.nz/ryegrassendophyte/endophyte-options.htm
  • Heritage Seeds. Seed guide [Internet]. 2018 [cited 2018 Sep 27]. Available from: https://www.heritageseeds.com.au/brochures-publications
  • Popay AJ, Hume DE, Baltus JG, Latch GCM, Tapper BA, Lyons TB, et al. Field performance of perennial ryegrass (Lolium perenne) infected with toxin-free fungal endophytes (Neotyphodium spp.). Grassland Research and Practice Series. 1999;7:113–122.
  • Popay AJ, Baltus JG. Black beetle damage to perennial ryegrass infected with AR 1 endophyte. Proceedings of the New Zealand Grassland Association. 2001;63:267–271.
  • Hunt MG, Newman JA. Reduced herbivore resistance from a novel grass–endophyte association. J Appl Ecol. 2005;42:762–769. https://doi.org/10.1111/j.1365-2664.2005.01061.x
  • Timper P, Bouton JH. Effect of endophyte status and tall fescue cultivar on reproduction of lesion and stubby-root nematodes. In: Kallenbach R, Rosenkrans C Jr, Lock TR, editors. Proceedings of the 5th International Symposium on Neotyphodium/Grass Interactions, 2004 May 23–26; Fayetteville, AR, USA. Fayetteville, AR: University of Arkansas; 2004. Poster No. 406.
  • Malinowski DP, Kigel J, Pinchak WE. Water deficit, heat tolerance, and persistence of summer-dormant grasses in the U.S. Southern Plains. Crop Sci. 2009;49:2363–2370. https://doi.org/10.2135/cropsci2009.06.0316
  • Ju HJ, Hill NS, Abbot T, Ingram KT. Temperature influences on endophyte growth in tall fescue. Crop Sci. 2006;46:404–412. https://doi.org/10.2135/cropsci2005.0282
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