Endophyte symbiosis with tall fescue: how strong are the impacts on communities and ecosystems?

Fungal Biology Reviews

Volumn 21, Issue 2-3, 2007, Pages 107-124

  Rudgers, Jennifer A ^a   Clay, Keith ^b  

^a RICE UNIVERSITY   (United States)

^b INDIANA UNIVERSITY   (United States)

Author keywords

Competition; Herbivory; Lolium arundinaceum; MAXQ endophyte; Neotyphodium coenophialum; Predators; Soil; Trophc interactions

Indexed keywords

ARTHROPODA; FESTUCA ARUNDINACEA; LOLIUM; NEOTYPHODIUM COENOPHIALUM;

EID: 34548646346     PISSN: 17494613     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.fbr.2007.05.002     Document Type: Review

References (135)

1. Agee C.S., and Hill N.S. Ergovaline variability in Acremonium-infected tall fescue due to environment and plant genotype. Crop Science 34 (1994) 221-226
2. Ball D.M., Pedersen J.F., and Lacefield G.D. The tall fescue endophyte. American Scientist 81 (1993) 370-379
3. Ball O.J.P., Pless C., and Gwinn K.D. Corn flea beetle (Chaetoncnema pulicaria) responses to natural endophytes of tall fescue, meadow fescue, and perennial ryegrass. In: Bacon C.W., and Hill N.S. (Eds). Neotyphodium/Grass Interactions (1997), Plenum Press, New York 243-246
4. Barger J.L., and Tannenbaum M.G. Consumption of endophyte-infected fescue seeds and osmoregulation in white-footed mice. Journal of Mammalogy 79 2 (1998) 464-474
5. Bazely D.R., Vicari M., Emmerich S., Filip L., Lin D., and Inman A. Interactions between herbivores and endophyte-infected Festuca rubra from the Scottish islands of St. Kilda, Benbecula and Rum. Journal of Applied Ecology 34 (1997) 847-860
6. Bernard E.C., Gwinn K.D., Pless C.D., and Williver C.L. Soil invertebrate species diversity and abundance in endophyte-infected tall fescue pastures. In: Bacon C.W., and Hill N.S. (Eds). Neotyphodium/grass interactions (1997), Plenum Press, New York 125-136
7. Boning R.A., and Bultman T.L. A test for constitutive and induced resistance by tall fescue (Festuca arundinacea) to an insect herbivore: Impact of fungal endopthte, Acremonium coenophialum. American Midland Naturalist 136 2 (1996) 328-335
8. Bouton J.H., Latch G.C.M., Hill N.S., Hoveland C.S., McCann M.A., Watson R.H., Parish J.A., Hawkins L.L., and Thompson F.N. Reinfection of tall fescue cultivars with non-ergot alkaloid-producing endophytes. Agronomy Journal 94 (2002) 567-574
9. Breen J.P. Acremonium/ endophyte interactions with enhanced plant resistance to insects. Annual Review of Entomology 39 (1994) 402-423
10. Bultman T.L., and Bell G.D. Interaction between fungal endophytes and environmental stressors influences plant resistance to insects. Oikos 103 1 (2003) 182-190
11. Bultman T.L., and Conard N.J. Effects of endophytic fungus, nutrient level, and plant damage on performance of all fall armyworm (Lepidoptera: Noctuidae). Environmental Entomology 27 3 (1998) 631-635
12. Bultman T.L., Borowicz K.L., Schneble R.M., Coudron T.A., and Bush L.P. Effect of a fungal endophyte on the growth and survival of two Euplectrus parasitoids. Oikos 78 1 (1997) 170-176
13. Bultman T.L., Bell G., and Martin W.D. A fungal endophyte mediates reversal of wound-induced resistance and constrains tolerance in a grass. Ecology 85 3 (2004) 679-685
14. Bultman T.L., Borowicz K.L., Schneble R.M., Coudron T.A., and Bush L.P. Effect of a fungal endophyte on the growth and survival of two Euplectrus parasitoids. Oikos 78 (1997) 170-176
15. Bush L.P., Wilkinson H.H., and Schardl C.L. Bioprotective alkaloids of grass-fungal endophyte symbioses. Plant Physiology 114 (1997) 1-7
16. Clement S.L., Lester D.G., Wilsokn A.D., Johnson R.C., and Bouton J.H. Expression of Russian wheat aphid (Homoptera: Aphididae) resistance in genotypes of tall fescue harboring different isolates of Acremonium endophyte. Journal of Economic Entomology 89 3 (1996) 766-770
17. Cheplick G.P. Genotypic variation in the regrowth of Lolium perenne following clipping: Effects of nutrients and endophytic fungi. Functional Ecology 12 (1998) 176-184
18. Cheplick G.P. Recovery from drought stress in Lolium perenne (Poaceae): Are fungal endophytes detrimental. American Journal of Botany 91 (2004) 1960-1968
19. Cheplick G.P. Symbiotic fungi and clonal plant physiology. New Phytologist 164 (2004) 413-415
20. Cheplick G.P., and Cho R. Interactive effects of fungal endophyte infection and host genotype on growth and storage in Lolium perenne. New Phytologist 158 (2003) 183-191
21. Cheplick G.P., Clay K., and Marks S. Interactions between infection by endophytic fungi and nutrient limitation in the grasses Lolium perenne and Festuca arundinacea. New Phytologist 111 (1989) 89-98
22. Christensen M.J., Ball O.J.P., Bennett R.J., and Schardl C.L. Fungal and host genotype effects on compatibility and vascular colonization by Epichloe festucae. Mycological Research 101 (1997) 493-501
23. Chu-chou M., Guo G., An Z.Q., Hendrix J.W., Ferris R.S., Siegel M.R., Dougherty C.T., and Burrus B.P. Suppression of mycorrhizal fungi in fescue by the Acremonium coenophialum endophyte. Soil Biology and Biochemistry 24 (1992) 633-637
24. Clay K. Fungal endophytes of grasses: a defensive mutualism between plants and fungi. Ecology 69 (1988) 10-16
25. Clay K. Interactions among fungal endophytes, grasses and herbivores. Researches on Population Ecology 38 (1996) 191-201
26. Clay K. Fungal endophytes, herbivores and the structure of grassland communities. In: Gange A.C., and Brown V.K. (Eds). Multitrophic interactions in terrestrial systems (1997), Blackwell, Oxford 151-169
27. Clay K., and Cheplick G.P. Effect of ergot alkaloids from fungal endophyte-infected grasses on fall armyworm (Spodoptera frugiperda). Journal of Chemical Ecology 15 (1989) 169-182
28. Clay K., and Holah J. Fungal endophyte symbiosis and plant diversity in successional fields. Science 285 (1999) 1742-1744
29. Clay K., Holah J., and Rudgers J.A. Herbivores cause a rapid increase in hereditary symbiosis and alter plant community composition. Proceedings of the National Academy of Sciences U. S. A 102 (2005) 12465-12470
30. Clay K., and Leuchtmann A. Infection of woodland grasses by fungal endophytes. Mycologia 81 (1989) 805-811
31. Clay K., Marks S., and Cheplick G.P. Effects of insect herbivory and fungal endophyte infection on competitive interactions among grasses. Ecology 74 (1993) 1767-1777
32. Clay K., and Schardl C. Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. American Naturalist 160 (2002) S99-S127
33. Clement S.L., Kaiser W.J., and Eichenseer H. Acremonium endophytes in germplasms of major grasses and their utilization for insect resistance. In: Bacon C.W., and White Jr. J.F. (Eds). Biotechnology of Endophytic Fungi of Grasses (1994), CRC Press, Boca Raton 185-199
34. Coley A.B., Fribourg H.A., Pelton M.R., and Gwinn K.D. Effects of tall fescue infestation on relative abundance of small mammals. Journal of Environmental Quality 24 (1995) 472-475
35. Conover M.R. Impact of consuming tall fescue leaves with the endophytic fungus, Acremonium coenophialum on meadow voles. Journal of Mammalogy 79 2 (1998) 457-463
36. Conover M.R., and Messmer T.A. Feeding preferences and changes in mass of Canada geese grazing endophyte-infected tall fescue. Auk 98 (1996) 859-862
37. Craven K.D., Blankenship J.D., Leuchtmann A., Hignight K., and Schardl C.L. Hybrid fungal endophytes symbiotic with the grass Lolium pratense. Sydowia 53 (2001) 44-73
38. Craven K.D., Hsiau P.T.W., Leuchtmann A., Hollin W., and Schardl C.L. Multigene phylogeny of Epichloe species, fungal symbionts of grasses. Annals of the Missouri Botanical Garden 88 (2001) 14-34
39. Dahlman D.L., Eichenseer H., and Siegel M.R. Chemical perspectives on endophyte-grass interactions and their implications to insect herbivory. In: Jones C., Krischik V., and Barbosa P. (Eds). Microorganisms, Plants and Herbivores (1991), John Wiley and Sons, New York 227-252
40. Davidson A.W., and Potter D.A. Response of plant-feeding, predatory, and soil-inhabiting invertebrates to Acremonium endophyte and nitrogen fertilization in tall fescue turf. Journal of Economic Entomology 88 (1995) 367-379
41. De Battista J.P., Bouton J.H., Bacon C.W., and Siegel M.R. Rhizome and herbage production of endophyte-removed tall fescue clones and populations. Agronomy Journal 82 (1990) 651-654
42. Dougherty C.T., Knapp F.W., and Bush L.P. Mortality of horn fly larvae (Diptera: Muscidae) in bovine dung supplemented with ergotamine and N-formyl Iodine. Journal of Medical Entomology 36 1 (1999) 73-77
43. Durham W.F., and Tannenbaum M.G. Effects of endophyte consumption on food intake, growth, and reproduction in prairie voles. Canadian Journal of Zoology 76 5 (1998) 960-969
44. Elmi A.A., West C.P., Robbins R.T., and Kirkpatrick T.L. Endophyte effects on reproduction of a root-knot nematode (Meloidogyne marylandi) and osmotic adjustment in tall fescue. Grass and Forage Science 55 2 (2000) 166-172
45. Faeth S.H., Gardner D.R., Hayes C.J., Jani A., Wittlinger S.K., and Jones T.A. Temporal and spatial variation in alkaloid levels in Achnatherum robustum, a native grass infected with the endophyte Neotyphodium. Journal of Chemical Ecology 32 (2006) 307-324
46. Faeth S.H., Helander M.L., and Saikkonen K. Asexual Neotyphodium endophytes in a native grass reduce competitive abilities. Ecology Letters 7 (2004) 304-313
47. Faeth S.H., and Sullivan T.J. Mutualistic asexual endophytes in a native grass are usually parasitic. American Naturalist 161 (2003) 310-325
48. Filipov N.M., Thompson F.N., Hill N.S., Dawe D.L., Stuedemann J.A., Price J.C., and Smith C.K. Vaccination against ergot alkaloids and the effect of endophyte-infected fescue seed-based diets on rabbits. Journal of Animal Science 76 9 (1998) 2456-2463
49. Finkes L.K., Cady A.B., Mulroy J.C., Clay K., and Rudgers J.A. Plant-fungus mutualism affects spider composition in successional fields. Ecology Letters 9 (2006) 347-356
50. Fortier G.M., Bard N., Jansen M., and Clay K. Effects of tall fescue endophyte infection and population density on growth and reproduction in prairie voles. Journal of Wildlife Management 64 1 (2000) 122-128
51. Fortier G.M., Osmon M.A., Roach M., and Clay K. Are female voles food limited? Effects of endophyte-infected tall fescue on home range size in female prairie voles (Microtus ochrogaster). American Midland Naturalist 146 1 (2001) 63-71
52. Fountain M.T., and Hopkin S.P. Folsomia candida (Collembola): A "standard" soil arthropod. Annual Review of Entomology 50 (2005) 201-222
53. Francis S.M., and Baird D.B. Increase in the proportion of endophyte-infected perennial ryegrass plants in overdrilled pastures. New Zealand Journal of Agricultural Research 32 (1989) 437-440
54. Franzluebbers A.J. Short-term responses of soil C and N fractions to tall fescue endophyte infection. Plant and Soil 282 (2006) 153-164
55. Franzluebbers A.J., and Hill N.S. Soil carbon, nitrogen, and ergot alkaloids with short- and long-term exposure to endophyte-infected and endophyte-free tall fescue. Soil Science Society of America Journal 69 (2005) 404-412
56. Franzluebbers A.J., Nazih N., Stuedemann J.A., Fuhrmann J.J., Schomberg H.H., and Hartel P.G. Soil carbon and nitrogen pools under low- and high-endophyte-infected tall fescue. Soil Science Society of America Journal 63 (1999) 1687-1694
57. Franzluebbers A.J., and Stuedemann J.A. Soil carbon and nitrogen pools in response to tall fescue endophyte infection, fertilization, and cultivar. Soil Science Society of America Journal 69 (2005) 396-403
58. Grewal S.K., Grewal P.S., and Gaugler R. Endophytes of fescue grasses enhances susceptibility of Popillia japonica larvae to an entomopathogenic nematode. Entomologia Experimentalis et Applicats 74 (1995) 219-224
59. Gwinn K.D., Collins-Shepard M.H., and Reddick B.B. Tissue print-immunoblot, an accurate method for the detection of Acremonium coenophialum in tall fescue. Phytopathology 81 (1991) 747-748
60. Hedges L.V., Gurevitch J., and Curtis P.S. The meta-analysis of response ratios in experimental ecology. Ecology 80 (1999) 1150-1156
61. Hiatt E.E., Hill N.S., Bouton J.H., and Stuedemann J.A. Tall fescue endophyte detection: Commercial immunoblot test kit compared with microscopic analysis. Crop Science 39 (1999) 796-799
62. Hiatt E.E., Hill N.S., and Hiatt E.N. Monoclonal antibodies incorporated into Neotyphodium coenophialum fungal cultures: Inhibition of fungal growth and stability of antibodies. Fungal Genetics and Biology 33 (2001) 107-114
63. Hiatt E.E., and Hill N.S. Neotyphodium coenophialum mycelial protein and herbage mass effects on ergot alkaloid concentration in tall fescue. Journal of Chemical Ecology 23 (1997) 2721-2736
64. Hill N.S., Hiatt E.E., De Battista J.P., Costa M.C., Griffiths C.H., Klap J., Thorogood D., and Reeves J.H. Seed testing for endophytes by microscopic and immunoblot procedures. Seed Science and Technology 30 (2002) 347-355
65. Hill N.S., Parrott W.A., and Pope D.D. Ergopeptine alkaloid production by endophytes in a common tall fescue genotype. Crop Science 31 (1991) 1545-1547
66. Hooper D.U., and Vitousek P.M. The effects of plant composition and diversity on ecosystem processes. Science 277 (1997) 1302-1305
67. Humphries S.S., Gwinn K.D., and Stewart A.J. Effects of endophyte status of tall fescue tissues on the earthworm (Eisenia fetida). Environmental Toxicology and Chemistry 20 6 (2001) 1346-1350
68. Hunt M.G., and Newman J.A. Reduced herbivore resistance from a novel grass-endophyte association. Journal of Applied Ecology 42 4 (2005) 762-769
69. Kimmons C.A., Gwinn K.D., and Bernard E.C. Nematode reproduction on endophyte-infected and endophyte-free tall fescue. Plant Disease 74 (1990) 757-761
70. Koga H., Hirai Y., Kanda K., Tsukiboshi T., and Uematsu T. Successive transmission of resistance to bluegrass webworm to perennial ryegrass and tall fescue plants by artifical inoculation with Acremonium endophytes. Jarq-Japan Agricultural Research Quarterly 31 2 (1997) 109-115
71. Koppenhofer A.M., Cowles R.S., and Fuzy E.M. Effects of turfgrass endophytes (Clavicipitaceae: Ascomycetes) on white grub (Coleoptera: Scarabaeidae) larval development and field populations. Environmental Entomology 32 4 (2003) 895-906
72. Koulman A., Lane G.A., Christensen M.J., Fraser K., and Tapper B.A. Peramine and other fungal alkaloids are exuded in the guttation fluid of endophyte-infected grasses. Phytochemistry 68 (2007) 355-360
73. Kucht S., Grob J., Hussein Y., Grothe T., Keller U., Basar S., Konig W.A., Steiner U., and Leister E. Elimination of ergoline alkaloids following treatment of Ipomoea asarifolia (Convolvulaceae) with fungicides. Planta 219 (2004) 619-625
74. Latch G.C.M. Physiological interactions of endophytic fungi and their hosts: Biotic stress tolerance imparted to grasses by endophytes. Agriculture Ecosystems & Environment 44 (1993) 143-156
75. Latch G.C.M., Potter L.R., and Tyler B.F. Incidence of endophytes in seeds from collections of Lolium and Festuca species. Annals of Applied Biology 111 (1987) 59-64
76. Lemons A., Clay K., and Rudgers J.A. Connecting plant-microbial interactions above and belowground: a fungal endophyte affects decomposition. Oecologia 145 4 (2005) 595-604
77. Leuchtmann A. Systematics, distribution, and host specificity of grass endophytes. Natural Toxins 1 (1992) 150-162
78. Leuchtmann A., and Clay K. Experimental evidence for genetic variation in compatibility between the fungus Atkinsonella hypoxylon and its three host grasses. Evolution 43 (1989) 825-834
79. Leuchtmann A., and Clay K. Morphological, cultural and mating studies on Atkinsonella, including Atkinsonella texensis new status. Mycologia 81 (1989) 692-701
80. Leuchtmann A., and Clay K. Isozyme variation in the Acremonium/Epichloe fungal endophyte complex. Phytopathology 80 (1990) 1133-1139
81. Leuchtmann A., Schmidt D., and Bush L.P. Different levels of protective alkaloids in grasses with stroma-forming and seed-transmitted Epichloe/Neotyphodium endophytes. Journal of Chemical Ecology 26 (2000) 1025-1036
82. Malinowski D.P., Alloush G.A., and Belesky D.P. Evidence for chemical changes on the root surface of tall fescue in response to infection with the fungal endophyte Neotyphodium coenophialum. Plant and Soil 205 (1998) 1-12
83. Malinowski D.P., and Belesky D.P. Adaptations of endophyte-infected cool-season grasses to environmental stresses: Mechanisms of drought and mineral stress tolerance. Crop Science 40 (2000) 923-940
84. Marks S., and Lincoln D.E. Antiherbivore defence mutualism under elevated carbondioxide levels: A fungal endophyte and grass. Environmental Entomology 25 3 (1996) 618-623
85. Matthews J.W., and Clay K. Influence of fungal endophyte infection on plant-soil feedback and community interactions. Ecology 82 (2001) 500-509
86. Mc Leod A.R., Rey A., Newsham K.K., Lewis G.C., and Wolferstan P. Effects of elevated ultraviolet radiation and endophytic fungi on plants growth and insects feeding in Lolium perenne, Festuca rubra, F. arundinacea and F. pratensis. Journal of Photochemistry and Photobiology B Biology 62 6 (2001) 97-107
87. Miles C.O., Di Menna M.E., Jacobs S.W.L., Garthwaite I., Lane G.A., Prestidge R.A., Marshall S.L., Wilkinson H.H., Schardl C.L., Ball O.J.P., and Latch G.C.M. Endophytic fungi in indigenous Australasian grasses associated with toxicity to livestock. Applied and Environmental Microbiology 64 (1998) 601-606
88. Moon C.D., Craven K.D., Leuchtmann A., Clement S.L., and Schardl C.L. Prevalence of interspecific hybrids amongst asexual fungal endophytes of grasses. Molecular Ecology 13 (2004) 1455-1467
89. Moon C.D., Miles C.O., Jarlfors U., and Schardl C.L. The evolutionary origins of three new Neotyphodium endophyte species from grasses indigenous to the Southern Hemisphere. Mycologia 94 (2002) 694-711
90. Muegge M.A., Quisenberry S.S., Bates G.E., and Joost R.E. Influence of Acremonium infection and pesticide use on seasonal abundance of leafhoppers and froghoppers (Homoptera, Cicadellidae, Cercopidae) in tall fescue. Environmental Entomology 20 6 (1991) 1531-1536
91. Murphy J.A., Sun S., and Betts L.L. Endophyte-enhanced resistance to billbug (Coleoptera: Curculionidae), sod webworm (Lepidoptera; Pyralidae), and white grub (Coleoptera; Scarabaeidae) in tall fescue. Environmental Entomology 22 (1993) 699-703
92. Murphy J.C., and Bultman T.L. Effects of natural and artifical herbivory on endophyte-infected tall fescue, Festuca arundinacea and response by the aphid, Rhopalosiphum padi. In: Bacon C.W., and Hill N.S. (Eds). Neotyphodium/Grass Interactions (1997), Plenum Press, New York 187-190
93. Newman J.A., Abner M.L., Dado R.J., Gibson D.J., Brookings A., and Parsons A.J. Effects of elevated CO2, nitrogen and fungal endophyte-infection on tall fescue: growth, photosynthesis, chemical composition and digestibility. Global Change Biology 9 (2003) 425-437
94. Oliver J.B., Pless C.D., and Gwinn K.D. Effect of endophyte, Acremonium coenophialum, in "Kentucky 31" tall fescue, Festuca arundinacea, on survival of Popillia japonica. In: Quisenberry S.S., and Joost R.E. (Eds). Proceedings of the International Symposium on Acremonium/Grass Interactions (1990), Louisiana Agricultural Experimental Station, Baton Rouge, LA 173-175
95. Omacini M., Chaneton E.J., Ghersa C.M., and Muller C.B. Symbiotic fungal endophytes control insect host-parasite interaction webs. Nature 409 (2001) 78-81
96. Omacini M., Chaneton E.J., Ghersa C.M., and Otero P. Do foliar endophytes affect grass litter decomposition? A microcosm approach using Lolium multiflorum. Oikos 104 (2004) 581-590
97. Omacini M., Eggers T., Bonkowski M., Gange A.C., and Jones T.H. Leaf endophytes affect mycorrhizal status and growth of co-infected and neighbouring plants. Functional Ecology 20 (2006) 226-232
98. Orr S.P., Rudgers J.A., and Clay K. Invasive plants can inhibit native tree seedlings: Testing potential allelopathic mechanisms. Plant Ecology 181 (2005) 153-165
99. Pan J.J., and Clay K. Infection by the systemic fungus Epichloe glyceriae and clonal growth of its host grass Glyceria striata. Oikos 98 (2002) 37-46
100. Pan J.J., and Clay K. Infection by the systemic fungus Epichloe glyceriae alters clonal growth of its grass host, Glyceria striata. Proceedings of the Royal Society of London Series B Biological Sciences 270 (2003) 1585-1591
101. Panaccione D.G., Johnson R.D., Wang J., Young C.A., Damrongkool P., Scott B., and Schardl C.L. Elimination of ergovaline from a grass-Neotyphodium endophyte symbiosis by genetic modification of the endophyte. Proceedings of the National Academy of Sciences of the United States of America 98 (2001) 12820-12825
102. Pedersen J.F., Rodriguez-Kabana R., and Shelby R.A. Ryegrass cultivars and endophyte in tall fescue affect nematodes in grass and succeeding soybean. Agronomy Journal 80 (1988) 811-814
103. Pennell C., and Ball O.J.P. The effects of Neotyphodium endophytes in tall fescue on pasture mealy bug (Balanococcus poae). Proceedings of the 52nd N.Z. Plant Protection Conference 1999 (1999) 259-263
104. Popay A.J., and Bonos S.A. Biotic responses in endophytic grasses. In: Roberts C., West C.P., and Spiers D.A. (Eds). Neotyphodium in Cool-Season Grasses: Current Research and Applications (2005), Blackwell, Ames, IA 163-186
105. Rasmussen S., Parsons A.J., Bassett S., Christensen M.J., Hume D.E., Johnson L.J., Johnson R.D., Simpson W.R., Stacke C., Voisey C.R., Xue H., and Newman J.A. High nitrogen supply and carbohydrate content reduce fungal endophyte and alkaloid concentration in Lolium perenne. New Phytologist 173 (2007) 787-797
106. Rice J.S., Pinkerton B.W., Stringer W.C., and Undersander D.J. Seed production in tall fescue as affected by fungal endophyte. Crop Science 30 (1990) 1303-1305
107. Richmond D.S., Grewal P.S., and Cardina J. Competition between Lolium perenne and Digitaria sanguinalis: Ecological consequences for harbouring an endosymbiotic fungus. Journal of Vegetation Science 14 6 (2003) 835-840
108. Rudgers J.A., and Clay K. Fungal endophytes in terrestrial communities and ecosystems. In: Dighton E.J., Oudemans P., and White Jr. J.F. (Eds). The Fungal Community (2005), M. Dekker, New York 423-442
109. Rudgers J.A., Holah J., Orr S.P., and Clay K. Forest succession suppressed by an introduced plant-fungal symbiosis. Ecology 88 (2007) 18-25
110. Rudgers J.A., Koslow J.M., and Clay K. Endophytic fungi alter relationships between diversity and ecosystem properties. Ecology Letters 7 (2004) 42-51
111. Rudgers J.A., Mattingly W.B., and Koslow J.M. Mutualistic fungus promotes plant invasion into diverse communities. Oecologia 144 (2005) 463-471
112. Sabzalian M.R., Hatami B., and Mirlohi A., Mealybug, Phenococcus solani, and barley aphid, Sipha maydis, response to endophyte-infected tall and meadow fescues. Entomologia Experimentalis et Applicats 113 3 (2004) 205-209
113. Saikkonen K., Ahlholm J., Helander M., Lehtimaki S., and Niemelainen O. Endophytic fungi in wild and cultivated grasses in Finland. Ecography 23 (2000) 360-366
114. Shelby R.A., and Dalrymple L.W. Incidence and distribution of the tall fescue endophyte in the USA. Plant Disease 71 (1987) 783-786
115. Shelby R.A., and Dalrymple L.W. Long-term changes of endophyte infection in tall fescue stands. Grass and Forage Science 48 (1993) 356-361
116. Siegel M.R., Latch G.C.M., Bush L.P., Fannin F.F., Rowan D.D., Tapper B.A., Bacon C.W., and Johnson M.C. Fungal endophyte-infected grasses: Alkaloid accumulation and aphid response. Journal of Chemical Ecology 16 (1990) 3301-3316
117. Spyreas G., Gibson D.J., and Basinger M. Endophyte infection levels of native and naturalized fescues in Illinois and England. Journal of the Torrey Botanical Society 128 (2001) 25-34
118. Tannenbaum M.G., Seematter S.L., and Zimmerman D.M. Endophyte-infected and uninfected fescue seeds suppress white-footed mouse (Peromyscus leucopus) reproduction. American Midland Naturalist 139 1 (1998) 114-124
119. Thompson R.W., Fribourg H.A., and Reddick B.B. Sample intensity and timing for detecting Acremonium coenophialum incidence in tall fescue pastures. Agronomy Journal 81 (1989) 966-971
120. Tibbets T.M., and Faeth S.H. Neotyphodium endophytes in grasses: Deterrents or promoters of herbivory by leaf-cutting ants?. Oecologia 118 3 (1999) 297-305
121. Tilman D. The ecological consequences of changes in biodiversity: a search for general principles. Ecology 80 (1999) 1455-1474
122. Tilman D., Hill J., and Lehman C. Carbon-negative biofuels from low-input high-diversity grassland biomass. Science 314 (2006) 1598-1600
123. Timper P., Gates R.N., and Bouton J.H. Nematode reproduction in tall fescue infected with different endophyte strains. Phytopathology 91 (2001) S144
124. Timper P., Gates R.N., and Bouton J.H. Response of Pratylenchus spp. in tall fescue infected with different strains of the fungal endophyte Neotyphodium coenophialum. Nematology 7 (2005) 105-110
125. Tintjer T., and Rudgers J.A. Grass-herbivore interactions altered by strains of a native endophyte. New Phytologist 170 (2006) 513-521
126. Tsai H.F., Liu J.S., Staben C., Christensen M.J., Latch G.C.M., Siegel M.R., and Schardl C.L. Evolutionary diversification of fungal endophytes of tall fescue grass by hybridization with Epichloe species. Proceedings of the National Academy of Sciences of the United States of America 91 (1994) 2542-2546
127. Wei Y.K., Gao Y.B., Xu H., Su D., Zhang X., Wang Y.H., Lin F., Chen L., Nie L.Y., and Ren A.Z. Neotyphodium in native grasses in China and observations on endophyte/host interactions. Grass and Forage Science 61 (2006) 422-429
128. West C.P. Physiology and drought tolerance of endophyte-infected grasses. In: Bacon C.W., and White Jr. J.F. (Eds). Biotechnology of Endophytic Fungi of Grasses (1994), CRC Press, Boca Raton 87-101
129. West C.P., Izekor E., Oosterhuis D.M., and Robbins R.T. The effect of Acremonium coenophialum on the growth and nematode infestation of tall fescue. Plant and Soil 112 (1988) 3-6
130. White J.F., Halisky P.M., Sun S.C., Morgan-Jones G., and Funk C.R. Endophyte-host associations in grasses. XVI. Patterns of endophyte distribution in species of the tribe Agrostideae. American Journal of Botany 79 (1992) 472-477
131. Wilkinson H.H., Siegel M.R., Blankenship J.D., Mallory A.C., Bush L.P., and Schardl C.L. Contribution of fungal loline alkaloids to protection from aphids in a grass-endophyte mutualism. Molecular Plant-Microbe Interactions 13 (2000) 1027-1033
132. Williamson R.C., and Potter D.A. Turfgrass species and endophyte effects on survival, development, and feeding preference of black cutworms (Lepidoptera: Noctuidae). Journal of Economic Entomology 90 5 (1997) 1290-1299
133. Wilson A.D., Clement S.L., Kaiser W.J., and Lester D.G. First report of clavicipitaceous anamorphic endophytes in Hordeum species. Plant Disease 75 (1991) 215
134. Young C.A., Bryant M.K., Christensen M.J., Tapper B.A., Bryan G.T., and Scott B. Molecular cloning and genetic analysis of a symbiosis-expressed gene cluster for lolitrem biosynthesis from a mutualistic endophyte of perennial ryegrass. Molecular Genetics and Genomics 274 (2005) 13-29
135. Zabalgogeazcoa I., de Aldana B.R.V., Ciudad A.G., and Criado B.G. Fungal endophytes in grasses from semi-arid permanent grasslands of western Spain. Grass and Forage Science 58 (2003) 94-97