Exploring the potential of symbiotic fungal endophytes in cereal disease suppression

Biological Control

Volumn 63, Issue 2, 2012, Pages 69-78

  O'Hanlon, Karen A ^a   Knorr, Kamilla ^a   Jørgensen, Lise Nistrup ^a   Nicolaisen, Mogens ^a   Boelt, Birte ^a  

^a AARHUS UNIVERSITY   (Denmark)

Author keywords

Biological control; C3 cool season grasses; Cereals; Fungal endophytes; Neotyphodium; Pathogen suppression; Plant pathogens

Indexed keywords

NEOTYPHODIUM; POACEAE; UREDINALES;

EID: 84867658950     PISSN: 10499644     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biocontrol.2012.08.007     Document Type: Review

References (150)

1. Arnold A.E., Lutzoni F. Diversity and host range of foliar fungal endophytes: are tropical leaves biodiversity hotspots?. Ecology 2007, 88:541-549.
2. Arnold A.E., Mejia L.C., Kyllo D., Rojas E.I., Maynard Z., Robbins N., Herre E.A. Fungal endophytes limit pathogen damage in a tropical tree. Proceedings of the National Academy of Sciences of the United States of America 2003, 100:15649-15654.
3. Asseng S., Foster I., Turner N.C. The impact of temperature variability on wheat yields. Global Change Biology 2011, 17:997-1012.
4. Bacon C.W. Toxic endophyte-infected tall fescue and range grasses - historic perspectives. Journal of Animal Science 1995, 73:861-870.
5. Bacon C.W., Hinton D.M. Symptomless endophytic colonization of maize by Fusarium moniliforme. Canadian Journal of Botany 1996, 74:1195-1202.
6. Bacon C.W., Porter J.K., Robbins J.D., Luttrell E.S. Epichloe typhina from toxic tall fescue grasses. Applied and Environmental Microbiology 1977, 34:576-581.
7. Bacon C.W., White J.F. Microbial Endophytes 2000, Dekker, New York, pp. 341-388.
8. Bishop D.L., Levine H.G., Kropp B.R., Anderson A.J. Seedborne fungal contamination: consequences in space-grown wheat. Phytopathology 1997, 87:1125-1133.
9. Bolton M.D., Kolmer J.A., Garvin D.F. Wheat leaf rust caused by Puccinia triticina. Molecular Plant Pathology 2008, 9:563-575.
10. Bonos S.A., Wilson M.M., Meyer W.A., Reed Funk C. Suppression of red thread in fine fescues through endophyte-mediated resistance. Applied Turfgrass Science Online Publication 2005, 10.1094/ATS-2005-0725-01-RS.
11. Bottalico A., Perrone G. Toxigenic Fusarium species and mycotoxins associated with head blight in small-grain cereals in Europe. European Journal of Plant Pathology 2002, 108:611-624.
12. Bush L.P., Wilkinson H.H., Schardl C.L. Bioprotective alkaloids of grass-fungal endophyte symbioses. Plant Physiology 1997, 114:1-7.
13. Cheplick G.P. Population Biology of Grasses 1998, Cambridge University Press, Cambridge.
14. Cheplick G.P., Faeth S.H. Ecology and Evolution of the Grass-endophyte Symbiosis 2009, Oxford University Press, New York.
15. Christensen M.J. Variation in the ability of Acremonium endophytes of Lolium perenne, Festuca arundinacea and F. pratensis to form compatible associations in the 3 grasses. Mycological Research 1995, 99:466-470.
16. Christensen M.J. Antifungal activity in grasses infected with Acremonium and Epichloe endophytes. Australasian Plant Pathology 1996, 25:186-191.
17. Christensen M.J., Bennett R.J., Schmid J. Growth of Epichloe/Neotyphodium and p-endophytes in leaves of Lolium and Festuca grasses. Mycological Research 2002, 106:93-106.
18. Clark, B., Nistrup Jørgensen, L., 2009. Strategies to control fusarium ear blight and mycotoxin production in wheat. ENDURE Wheat Case Study - Guide Number 2.
19. Clarke B.B., White J.F., Hurley R.H., Torres M.S., Sun S., Huff D.R. Endophyte-mediated suppression of dollar spot disease in fine fescues. Plant Disease 2006, 90:994-998.
20. Clay K. Clavicipitaceous endophytes of grasses - their potential as biocontrol agents. Mycological Research 1989, 92:1-12.
21. Clay K., Schardl C. Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. American Naturalist 2002, 160:S99-S127.
22. Crous P.W., Petrini O., Marais G.F., Pretorius Z.A., Rehder F. Occurrence of fungal endophytes in cultivars of Triticum aestivum in South Africa. Mycoscience 1995, 36:105-111.
23. D'Mello J.P.F., Placinta C.M., Macdonald A.M.C. Fusarium mycotoxins: a review of global implications for animal health, welfare and productivity. Animal Feed Science and Technology 1999, 80:183-205.
24. Danielsen S., Jensen D.F. Fungal endophytes from stalks of tropical maize and grasses: isolation, identification, and screening for antagonism against Fusarium verticillioides in maize stalks. Biocontrol Science and Technology 1999, 9:545-553.
25. Dingle J., McGee P.A. Some endophytic fungi reduce the density of pustules of Puccinia recondita f. sp tritici in wheat. Mycological Research 2003, 107:310-316.
26. Dodds P.N., Rathjen J.P. Plant immunity: towards an integrated view of plant-pathogen interactions. Nature Reviews Genetics 2010, 11:539-548.
27. Eaton C.J., Cox M.P., Ambrose B., Becker M., Hesse U., Schardl C.L., Scott B. Disruption of signaling in a fungal-grass symbiosis leads to pathogenesis. Plant Physiology 2010, 153:1780-1794.
28. Eaton C.J., Cox M.P., Scott B. What triggers grass endophytes to switch from mutualism to pathogenism?. Plant Science 2011, 180:190-195.
29. Engle J.S., Madden L.V., Lipps P.E. Evaluation of inoculation methods to determine resistance reactions of wheat to Fusarium graminearum. Plant Disease 2003, 87:1530-1535.
30. Estrada A.E.R., Hegeman A., Kistler H.C., May G. In vitro interactions between Fusarium verticillioides and Ustilago maydis through real-time PCR and metabolic profiling. Fungal Genetics and Biology 2011, 48:874-885.
31. Faeth S.H. Are endophytic fungi defensive plant mutualists?. Oikos 2002, 98:25-36.
32. Faeth S.H., Fagan W.F. Fungal endophytes: common host plant symbionts but uncommon mutualists. Integrative and Comparative Biology 2002, 42:360-368.
33. Faeth S.H., Gardner D.R., Hayes C.J., Jani A., Wittlinger S.K., 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 2006, 32:307-324.
34. Faeth S.H., Sullivan T.J. Mutualistic asexual endophytes in a native grass are usually parasitic. American Naturalist 2003, 161:310-325.
35. Fisher M.C., Henk D.A., Briggs C.J., Brownstein J.S., Madoff L.C., McCraw S.L., Gurr S.J. Emerging fungal threats to animal, plant and ecosystem health. Nature 2012, 484:186-194.
36. Fisher P.J., Petrini O. Fungal saprobes and pathogens as endophytes of rice (Oryza sativa L). New Phytologist 1992, 120:137-143.
37. Gill, B.S., 2010. Compendium of wheat diseases and pests. In: Bockus, B., Hunger, Murray, Smiley (Eds.), Springer The American Phytopathological Society, USA, 1-4.
38. Gladders, P., 2008. Pest Disease and Weed Incidence Report, Harvest Year 2008. Agricultural Development and Advisory Service, U.K., pp. 58.
39. Gladders P., Langton S.D., Barrie I.A., Hardwick N.V., Taylor M.C., Paveley N.D. The importance of weather and agronomic factors for the overwinter survival of yellow rust (Puccinia striiformis) and subsequent disease risk in commercial wheat crops in England. Annals of Applied Biology 2007, 150:371-382.
40. Gladders P., Paveley N.D., Barrie I.A., Hardwick N.V., Hims M.J., Langton S., Taylor M.C. Agronomic and meteorological factors affecting the severity of leaf blotch caused by Mycosphaerella graminicola in commercial wheat crops in England. Annals of Applied Biology 2001, 138:301-311.
41. Glawe D.A. The powdery mildews: a review of the world's most familiar (yet poorly known) plant pathogens. Annual Review of Phytopathology 2008, 46:27-51.
42. Godfray H.C.J., Beddington J.R., Crute I.R., Haddad L., Lawrence D., Muir J.F., Pretty J., Robinson S., Thomas S.M., Toulmin C. Food Security: the challenge of feeding 9 billion people. Science 2010, 327:812-818.
43. Gunter S.A., Beck P.A. Novel endophyte-infected tall fescue for growing beef cattle. Journal of Animal Science 2004, 82:E75-E82. (E-Suppl).
44. Gutteridge R.J., Bateman G.L., Todd A.D. Variation in the effects of take-all disease on grain yield and quality of winter cereals in field experiments. Pest Management Science 2003, 59:215-224.
45. Gwinn K.D., Gavin A.M. Relationship between endophyte infestation level of tall fescue seed lots and Rhizoctonia zeae seedling disease. Plant Disease 1992, 76:911-914.
46. Hahn H., McManus M.T., Warnstorff K., Monahan B.J., Young C.A., Davies E., Tapper B.A., Scott B. Neotyphodium fungal endophytes confer physiological protection to perennial ryegrass (Lolium perenne L.) subjected to a water deficit. Environmental and Experimental Botany 2008, 63:183-199.
47. Hanada R.E., Pomella A.W.V., Costa H.S., Bezerra J.L., Loguercio L.L., Pereira J.O. Endophytic fungal diversity in Theobroma cacao (cacao) and T. grandiflorum (cupuacu) trees and their potential for growth promotion and biocontrol of black-pod disease. Fungal Biology 2010, 114:901-910.
48. Hanada R.E., Pomella A.W.V., Soberanis W., Loguercio L.L., Pereira J.O. Biocontrol potential of Trichoderma martiale against the black-pod disease (Phytophthora palmivora) of cacao. Biological Control 2009, 50:143-149.
49. Hanada R.E., Souza T.D., Pomella A.W.V., Hebbar K.P., Pereira J.O., Ismaiel A., Samuels G.J. Trichoderma martiale sp nov., a new endophyte from sapwood of Theobroma cacao with a potential for biological control. Mycological Research 2008, 112:1335-1343.
50. Hensel G., Himmelbach A., Chen W.X., Douchkov D.K., Kumlehn J. Transgene expression systems in the Triticeae cereals. Journal of Plant Physiology 2011, 168:30-44.
51. Herrera J., Khidir H.H., Eudy D.M., Porras-Alfaro A., Natvig D.O., Sinsabaugh R.L. Shifting fungal endophyte communities colonize Bouteloua gracilis: effect of host tissue and geographical distribution. Mycologia 2010, 102:1012-1026.
52. Hochholdinger F., Tuberosa R. Genetic and genomic dissection of maize root development and architecture. Current Opinion in Plant Biology 2009, 12:172-177.
53. Hovmoller M.S., Sorensen C.K., Walter S., Justesen A.F. Diversity of Puccinia striiformis on Cereals and Grasses. Annual review of Phytopathology 2011, 49:197-217.
54. Ikeda S., Okubo T., Kaneko T., Inaba S., Maekawa T., Eda S., Sato S., Tabata S., Mitsui H., Minamisawa K. Community shifts of soybean stem-associated bacteria responding to different nodulation phenotypes and N levels. Isme Journal 2010, 4:315-326.
55. Istifadah N., McGee P.A. Endophytic Chaetomium globosum reduces development of tan spot in wheat caused by Pyrenophora tritici-repentis. Australasian Plant Pathology 2006, 35:411-418.
56. Johnson M.C., Bush L.P., Siegel M.R. Infection of tall fescue with Acremonium coenophialum by means of callus culture. Plant Disease 1986, 70:380-382.
57. Jumpponen A., Trappe J.M. Dark septate endophytes: a review of facultative biotrophic root-colonizing fungi. New Phytologist 1998, 140:295-310.
58. Jørgensen L.N., Nielsen G.C., Ørum J.E., Jensen J.E., Pinnschmidt H.O. Integrating Disease Control in Winter Wheat - Optimizing Fungicide Input. Outlooks on Pest Management 2008, 8(5):206-213.
59. Jørgensen L.N., Olsen L.V. Control of tan spot (Drechslera tritici-repentis) using host resistance-power. Methods and fungicides. Crop Protection 2007, 11.
60. Kiss L. A review of fungal antagonists of powdery mildews and their potential as biocontrol agents. Pest Management Science 2003, 59:475-483.
61. Koga H., Christensen M.J., Bennett R.J. Incompatibility of some grass-Acremonium endophyte associations. Mycological Research 1993, 97:1237-1244.
62. Kolmer J.A. Tracking wheat rust on a continental scale. Current Opinion in Plant Biology 2005, 8:441-449.
63. Kuck K.H., Gisi U. FRAC mode of action classification and resistance risk of fungicides. Modern Crop Protection Compounds 2006, 415-432. Wiley-VCH verlag. K. Schirmer (Ed.).
64. Kuldau G., Bacon C. Clavicipitaceous endophytes: their ability to enhance resistance of grasses to multiple stresses. Biological Control 2008, 46:57-71.
65. Kuldau G.A., Liu J.S., White J.F., Siegel M.R., Schardl C.L. Molecular systematics of Clavicipitaceae supporting monophyly of genus Epichloe and form genus Ephelis. Mycologia 1997, 89:431-441.
66. Lambert M.G., Clark D.A., Litherland A.J. Advances in pasture management for animal productivity and health. New Zealand Veterinary Journal 2004, 52:311-319.
67. Larran S., Perello A., Simon M.R., Moreno V. Isolation and analysis of endophytic microorganisms in wheat (Triticum aestivum L.) leaves. World Journal of Microbiology and Biotechnology 2002, 18:683-686.
68. Larran S., Perello A., Simon M.R., Moreno V. The endophytic fungi from wheat (Triticum aestivum L.). World Journal of Microbiology and Biotechnology 2007, 23:565-572.
69. Latch G.C.M. Physiological interactions of endophytic fungi and their hosts - biotic stress tolerance imparted to grasses by endophytes. Agriculture Ecosystems and Environment 1993, 44:143-156.
70. Latch G.C.M., Christensen M.J. Artificial infection of grasses with endophytes. Annals of Applied Biology 1985, 107:17-24.
71. Lee K., Pan J.J., May G. Endophytic Fusarium verticillioides reduces disease severity caused by Ustilago maydis on maize. Fems Microbiology Letters 2009, 299:31-37.
72. Leuchtmann A. Systematics, distribution, and host specificity of grass endophytes. Natural Toxins 1992, 1:150-162.
73. Lewandowski S.M., Bushnell W.R., Evans C.K. Distribution of mycelial colonies and lesions in field-grown barley inoculated with Fusarium graminearum. Phytopathology 2006, 96:567-581.
74. Li T., Liu M.J., Zhang X.T., Zhang H.B., Sha T., Zhao Z.W. Improved tolerance of maize (Zea mays L.) to heavy metals by colonization of a dark septate endophyte (DSE) Exophiala pisciphila. Science of the Total Environment 2011, 409:1069-1074.
75. Loyce C., Meynard J.M., Bouchard C., Rolland B., Lonnet P., Bataillon P., Bernicot M.H., Bonnefoy M., Charrier X., Debote B., Dernarquet T., Duperrier B., Felix I., Heddadj D., Leblanc O., Leleu M., Mangin P., Meausoone M., Doussinault G. Interaction between cultivar and crop management effects on winter wheat diseases, lodging, and yield. Crop Protection 2008, 27:1131-1142.
76. Lucas J.A., Dyer P.S., Murray T.D. Pathogenicity, host-specificity, and population biology of Tapesia spp., causal agents of eyespot disease of cereals. Advances in Botanical Research Incorporating Advances in Plant Pathology 2000, 33(33):225-258.
77. Lyons P.C., Plattner R.D., Bacon C.W. Occurrence of peptide and clavine ergot alkaloids in tall fescue grass. Science 1986, 232:487-489.
78. Macia-Vicente J.G., Jansson H.B., Mendgen K., Lopez-Llorca L.V. Colonization of barley roots by endophytic fungi and their reduction of take-all caused by Gaeumannomyces graminis var. tritici. Canadian Journal of Microbiology 2008, 54:600-609.
79. Macia-Vicente J.G., Rosso L.C., Ciancio A., Jansson H.B., Lopez-Llorca L.V. Colonisation of barley roots by endophytic Fusarium equiseti and Pochonia chlamydosporia: effects on plant growth and disease. Annals of Applied Biology 2009, 155:391-401.
80. Malinowski D.P., Belesky D.P. Adaptations of endophyte-infected cool-season grasses to environmental stresses: mechanisms of drought and mineral stress tolerance. Crop Science 2000, 40:923-940.
81. Manter D.K., Delgado J.A., Holm D.G., Stong R.A. Pyrosequencing reveals a highly diverse and cultivar-specific bacterial endophyte community in potato roots. Microbial Ecology 2010, 60:157-166.
82. Marshall D., Tunali B., Nelson L.R. Occurrence of fungal endophytes in species of wild Triticum. Crop Science 1999, 39:1507-1512.
83. McCallum B.D., Tekauz A. Influence of inoculation method and growth stage on Fusarium head blight in barley. Canadian Journal of Plant Pathology 2001, 24:77-80.
84. Molitor A., Zajic D., Voll L.M., Pons K.H.J., Samans B., Kogel K.H., Waller F. Barley leaf transcriptome and metabolite analysis reveals new aspects of compatibility and Piriformospora indica? Mediated systemic induced resistance to powdery mildew. Molecular Plant-Microbe Interactions 2011, 24:1427-1439.
85. Morganjones G., Gams W. Notes on Hyphomycetes.41. An endophyte of Festuca arundinacea and the anamorph of Epichloe typhina, new taxa in one of 2 new sections of Acremonium. Mycotaxon 1982, 15:311-318.
86. Morganjones G., White J.F., Piontelli E.L. Endophyte-host associations in forage grasses.8. Acremonium chilense, an undescribed endophyte occurring in Dactylis glomerata in Chile. Mycotaxon 1990, 39:441-454.
87. Muller C.B., Krauss J. Symbiosis between grasses and asexual fungal endophytes. Current Opinion in Plant Biology 2005, 8:450-456.
88. Naik B.S., Shashikala J., Krishnamurthy Y.L. Study on the diversity of endophytic communities from rice (Oryza sativa L.) and their antagonistic activities in vitro. Microbiological Research 2009, 164:290-296.
89. Narisawa K., Usuki F., Hashiba T. Control of Verticillium yellows in Chinese cabbage by the dark septate endophytic fungus LtVB3. Phytopathology 2004, 94:412-418.
90. Newsham K.K. A meta-analysis of plant responses to dark septate root endophytes. New Phytologist 2011, 190:783-793.
91. Newsham K.K., Upson R., Read D.J. Mycorrhizas and dark septate root endophytes in polar regions. Fungal Ecology 2009, 2:10-20.
92. Nicolaisen M., Suproniene S., Nielsen L.K., Lazzaro I., Spliid N.H., Justesen A.F. Real-time PCR for quantification of eleven individual Fusarium species in cereals. Journal of Microbiol Methods 2009, 234-240. (The Netherlands).
93. Nielsen L.K., Jensen J.D., Nielsen G.C., Jensen J.E., Spliid N.H., Thomsen I.K., Justesen A.F., Collinge D.B., Jorgensen L.N. Fusarium head blight of cereals in Denmark: species complex and related mycotoxins. Phytopathology 2011, 101(8):960-969.
94. Oerke E.C. Crop losses to pests. The Journal of Agricultural Science 2006, 144:31-43.
95. Pan J.J., Baumgarten A.M., May G. Effects of host plant environment and Ustilago maydis infection on the fungal endophyte community of maize (Zea mays). New Phytologist 2008, 178:147-156.
96. Parry D.W., Jenkinson P., McLeod L. Fusarium ear blight (scab) in small-grain cereals - a review. Plant Pathology 1995, 44:207-238.
97. Paulitz T.C. Take-all. Compendium of Wheat Diseases and Pests 2010, 79-82. The American Phytopathological Society, USA. Bockus, Bowden, Hunger, Morrill, Murray, smiley (Eds.).
98. Pennell C.G.L., Rolston M.P., De Bonth A., Simpson W.R., Hume D.E. Development of a bird-deterrent fungal endophyte in turf tall fescue. New Zealand Journal of Agricultural Research 2010, 53:145-150.
99. Petrini O. Taxonomy of endophytic fungi of aerial plant tissues. Microbio of the Phyllosphere 1986, 175-187. Cambridge University Press, Cambridge. N.J. Fokkema, J. van der Heuvel (Eds.).
100. Porras-Alfaro A., Bayman P. Hidden Fungi, Emergent Properties: Endophytes and Microbiomes. Annual Review of Phytopatholology 2010, 49:291-315.
101. Redman R.S., Sheehan K.B., Stout R.G., Rodriguez R.J., Henson J.M. Thermotolerance generated by plant/fungal symbiosis. Science 2002, 298:1581.
102. Reinhold-Hurek B., Hurek T. Living inside plants: bacterial endophytes. Current Opinion in Plant Biology 2011, (Published by Elsevier Ltd.).
103. Ren A.Z., Clay K. Impact of a horizontally transmitted endophyte, balansia henningsiana, on growth and drought tolerance of Panicum rigidulum. International Journal of Plant Sciences 2009, 170:599-608.
104. Rodriguez Estrada, A.E., Jonkers, W., Corby Kistler, H., May, G., 2012. Interactions between fusarium verticillioides, ustilago maydis, and zea mays: an endophyte, a pathogen, and their shared plant host. Fungal Genet Biol Springer Elsevier Inc, United States, pp. 578-587.
105. Rodriguez R.J., White J.F., Arnold A.E., Redman R.S. Fungal endophytes: diversity and functional roles. New Phytologist 2009, 182:314-330.
106. Rommens C.M., Kishore G.M. Exploiting the full potential of disease-resistance genes for agricultural use. Current Opinion in Biotechnology 2000, 11:120-125.
107. Saikkonen K., Helander M., Faeth S.H., Schulthess F., Wilson D. Endophyte-grass-herbivore interactions: the case of Neotyphodium endophytes in Arizona fescue populations. Oecologia 1999, 121:411-420.
108. Saikkonen K., Lehtonen P., Helander M., Koricheva J., Faeth S.H. Model systems in ecology: dissecting the endophyte-grass literature. Trends in Plant Science 2006, 11:428-433.
109. Saikkonen K., Wali P.R., Helander M. Genetic compatibility determines endophyte-grass combinations. Plos One 2010, 5(6):e11395.
110. Schafer P., Khatabi B., Kogel K.H. Root cell death and systemic effects of Piriformospora indica: a study on mutualism. FEMS Microbiol Lett 2007, 257(1):1-7.
111. Schardl C.L. Fungal Endophytes in Lolium and Festuca Species 2009, Springer, New York.
112. Schardl C.L., Grossman R.B., Nagabhyru P., Faulkner J.R., Mallik U.P. Loline alkaloids: currencies of mutualism. Phytochemistry 2007, 68:980-996.
113. Schardl C.L., Leuchtmann A., Spiering M.J. Symbioses of grasses with seedborne fungal endophytes. Annual Review of Plant Biology 2004, 55:315-340.
114. Schardl C.L., Panaccione D.G., Tudzynski P. Ergot alkaloids - biology and molecular biology. Alkaloids Chem Biol 2006, 63:45-86.
115. Schulz B., Boyle C. The endophytic continuum. Mycological Research 2005, 109:661-686.
116. Scott B. Epichloe endophytes: fungal symbionts of grasses. Current Opinion in Microbiology 2001, 4:393-398.
117. Serfling A., Wirsel S.G.R., Lind V., Deising H.B. Performance of the biocontrol fungus Piriformospora indica on wheat under greenhouse and field conditions. Phytopathology 2007, 97:523-531.
118. Shah J. Plants under attack: systemic signals in defence. Current Opinion in Plant Biology 2009, 12:459-464.
119. Shaner G. Septoria tritici Blotch. Compendium of Wheat Diseases and Pests 2010, 56-58. The American Phytopathological Society, USA. Bockus, Bowden, Hunger, Murray, Smiley (Eds.).
120. Sherameti I., Tripathi S., Varma A., Oelmuller R. The root-colonizing endophyte Pirifomospora indica confers drought tolerance in Arabidopsis by stimulating the expression of drought stress-related genes in leaves. Molecular Plant-Microbe Interactions 2008, 21:799-807.
121. Shittu H.O., Castroverde D.C.M., Nazar R.N., Robb J. Plant-endophyte interplay protects tomato against a virulent Verticillium. Planta 2009, 229:415-426.
122. Shoresh M., Harman G.E., Mastouri F. Induced systemic resistance and plant responses to fungal biocontrol agents. Annual Review of Phytopathology 2010, 48(48):21-43.
123. Sieber T., Riesen T.K., Muller E., Fried P.M. Endophytic fungi in four winter wheat cultivars (Triticum aestivum L.) differing in resistance against Stagonospora nodorum (Berk.) Cast. Germ.= Septoria nodorum Berk. Journal of Phytopathology-Phytopathologische Zeitschrift 1988, 122:289-306.
124. Siegel M.R., Latch G.C.M. Expression of antifungal activity in agar culture by isolates of grass endophytes. Mycologia 1991, 83:529-537.
125. Strickland J.R., Looper M.L., Matthews J.C., Rosenkrans C.F., Flythe M.D., Brown K.R. BOARD-INVITED REVIEW: St. Anthony's fire in livestock: causes, mechanisms, and potential solutions. Journal of Animal Science 2011, 89:1603-1626.
126. Stromberg E.L. Powdery Mildews. Compendium of wheat diseases and pests 2010, 43-45. The American Phytopathological Society, USA. B. Bockus, Hunger, Morrill, Murray, Smiley (Eds.).
127. Takemoto D., Kamakura S., Saikia S., Becker Y., Wrenn R., Tanaka A., Sumimoto H., Scott B. Polarity proteins Bem1 and Cdc24 are components of the filamentous fungal NADPH oxidase complex. Proc. Natl. Acad. Sci. USA 2011, 108(7):2861-2866.
128. Takemoto D., Tanaka A., Scott B. A p67(Phox)-like regulator is recruited to control hyphal branching in a fungal-grass mutualistic symbiosis. Plant Cell 2006, 18:2807-2821.
129. Tanaka A., Christensen M.J., Takemoto D., Park P., Scott B. Reactive oxygen species play a role in regulating a fungus-perennial ryegrass mutualistic interaction. Plant Cell 2006, 18:1052-1066.
130. Tanaka A., Takemoto D., Hyon G.S., Park P., Scott B. NoxA activation by the small GTPase RacA is required to maintain a mutualistic symbiotic association between Epichloe festucae and perennial ryegrass. Molecular Microbiology 2008, 68:1165-1178.
131. Tian P., Nan Z.B., Li C.J., Spangenberg G. Effect of the endophyte Neotyphodium lolii on susceptibility and host physiological response of perennial ryegrass to fungal pathogens. European Journal of Plant Pathology 2008, 122:593-602.
132. Tian X.L., Cao L.X., Tan H.M., Zeng Q.G., Jia Y.Y., Han W.Q., Zhou S.N. Study on the communities of endophytic fungi and endophytic actinomycetes from rice and their antipathogenic activities in vitro. World Journal of Microbiology and Biotechnology 2004, 20:303-309.
133. Vallino M., Greppi D., Novero M., Bonfante P., Lupotto E. Rice root colonisation by mycorrhizal and endophytic fungi in aerobic soil. Annals of Applied Biology 2009, 154:195-204.
134. van Zijll de Jong E., Guthridge K.M., Spangenberg G.C., Forster J.W. Sequence analysis of SSR-flanking regions identifies genome affinities between Pasture grass fungal endophyte taxa. International Journal of Evolutionary Biology 2011, 2011:921312.
135. Wali P.R., Helander M., Nissinen O., Saikkonen K. Susceptibility of endophyte-infected grasses to winter pathogens (snow molds). Canadian Journal of Botany-Revue Canadienne De Botanique 2006, 84:1043-1051.
136. Waller F., Achatz B., Baltruschat H., Fodor J., Becker K., Fischer M., Heier T., Huckelhoven R., Neumann C., von Wettstein D., Franken P., Kogel K.H. The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc. Natl. Acad. Sci. USA 2005, 102(38):13386-13391.
137. Walters D., Walsh D., Newton A., Lyon G. Induced resistance for plant disease control: maximizing the efficacy of resistance elicitors. Phytopathology 2005, 95:1368-1373.
138. Wegulo S.N., Breathnach J.A., Baenziger P.S. Effect of growth stage on the relationship between tan spot and spot blotch severity and yield in winter wheat. Crop Protection 2009, 28:696-702.
139. Wegulo S.N., Zwingman M.V., Breathnach J.A., Baenziger P.S. Economic returns from fungicide application to control foliar fungal diseases in winter wheat. Crop Protection 2011, 30:685-692.
140. Welty R.E., Barker R.E., Azevedo M.D. Reaction of tall fescue infected and noninfected by Acremonium coenophialum to Puccinia graminis subsp graminicola. Plant Disease 1991, 75:883-886.
141. White J.F. Endophyte-host associations in forage grasses.11. A proposal concerning origin and evolution. Mycologia 1988, 80:442-446.
142. White J.F., Cole G.T. Endophyte-host associations in forage grasses. 3. In vitro inhibition of fungi by Acremonium coenophialum. Mycologia 1985, 77:487-489.
143. White J.F., Cole G.T. Endophyte-host associations in forage grasses.4. The endophyte of Festuca versuta. Mycologia 1986, 78:102-107.
144. White J.F., Reddy P.V. Examination of structure and molecular phylogenetic relationships of some graminicolous symbionts in genera Epichloe and Parepichloe. Mycologia 1998, 90:226-234.
145. White J.F., Torres M.S. Is plant endophyte-mediated defensive mutualism the result of oxidative stress protection?. Physiologia Plantarum 2010, 138:440-446.
146. Wilson A.D., Clement S.L., Kaiser W.J. Endophytic fungi in a Hordeum germplasm collection. Plant Genetic Resources Newsletter 1992, 1-4.
147. Wilson D. Endophyte - the evolution of a term, and clarification of its use and definition. Oikos 1995, 73:274-276.
148. Yu L., Nicolaisen M., Larsen J., Ravnskov S. Molecular characterization of root-associated fungal communities in relation to health status of Pisum sativum using barcoded pyrosequencing. Plant Soil 2012, 357:395-405.
149. Yuan Z.L., Lin F.C., Zhang C.L., Kubicek C.P. A new species of Harpophora (Magnaporthaceae) recovered from healthy wild rice (Oryza granulata) roots, representing a novel member of a beneficial dark septate endophyte. Fems Microbiology Letters 2010, 307:94-101.
150. Zhang H.H., Tang M., Chen H., Wang Y.J. Effects of a dark-septate endophytic isolate LBF-2 on the medicinal plant Lycium barbarum L. Journal of Microbiology 2012, 50:91-96.