Susceptibility of tall fescue to Rhizoctonia zeae infection as affected by endophyte symbiosis

Annals of Applied Biology

Volumn 163, Issue 2, 2013, Pages 257-268

  Panka D ^a   West, C P ^b   Guerber, C A ^b   Richardson, M D ^b  

^a UNIVERSITY OF TECHNOLOGY AND LIFE SCIENCES   (Poland)

^b UNIVERSITY OF ARKANSAS   (United States)

Author keywords

Dual culture; endophyte; Lolium arundinaceum; mycelium density; Neotyphodium coenophialum; phenolic compounds; Rhizoctonia zeae

Indexed keywords

DISEASE; DISEASE SEVERITY; ENDOPHYTE; FUNGUS; HOST PLANT; INOCULATION; LEAF MORPHOLOGY; PHENOLIC COMPOUND; SYMBIOSIS;

BIPOLARIS SOROKINIANA; COCHLIOBOLUS LUNATUS; FESTUCA ARUNDINACEA; FUNGI; HYPHOMYCETES; LOLIUM; MYCELIUM (GENUS); NEOTYPHODIUM; NEOTYPHODIUM COENOPHIALUM; POACEAE; THANATEPHORUS CUCUMERIS; WAITEA CIRCINATA;

EID: 84882450170     PISSN: 00034746     EISSN: 17447348     Source Type: Journal    
DOI: 10.1111/aab.12051     Document Type: Article

References (83)

1. Ahlholm J.U., Helander M., Lechtimäki S., Wäli P., Saikkonen K., (2002) Vertically transmitted fungal endophytes: different responses of host-parasite systems to environmental conditions. Oikos, 99, 173-183.
2. Bolwell G.P., Bindschedler L.V., Blee K., Butt V.S., Davies D.R., Gardner S.L., Gerrish C., Minibayeva F., (2002) The apoplastic oxidative burst in response to biotic stress in plants: a three-component system. Journal of Experimental Botany, 53, 1367-1376.
3. Bonos S.A., Wilson M.M., Meyer W.A., Funk C.R., (2005) Suppression of red thread in fine fescues through endophyte-mediated resistance. Applied Turfgrass Science. DOI: 10.1094/ATS-2005-0725-01-RS.
4. Bouton J., Easton S., (2005) Endophytes in forage cultivars. In Neotyphodium in Cool-season Grasses, pp. 327-340. Eds, C.A. Roberts, C.P. West, and, D.E. Spiers,. Ames, IA, USA: Blackwell Publishing.
5. Brilman L.A., (2005) Endophytes in turfgrass cultivars. In Neotyphodium in Cool-season Grasses, pp. 341-349. Eds, C.A. Roberts, C.P. West, and, D.E. Spiers,. Ames, IA, USA: Blackwell Publishing.
6. Burnes J., Yokota T., Ashihara H., Lean M.E.J., Crozier A., (2002) Plant foods and herbal sources of resveratrol. Journal of Agricultural and Food Chemistry, 50, 3337-3340.
7. Burpee L.L., Bouton J.H., (1993) Effect of eradication of the endophyte Acremonium coenophialum on epidemics of Rhizoctonia blight in tall fescue. Plant Disease, 77, 157-159.
8. Burpee L.L., Martin B., (1992) Biology of Rhizoctonia species associated with turfgrasses. Plant Disease, 76, 112-117.
9. Campbell M.M., Ellis B.E., (1992) Fungal elicitor-mediated responses in pine cell cultures: cell wall-bound phenolics. Phytochemistry, 31, 737-742.
10. Cheplick G.P., (2004) Recovery from drought stress in Lolium perenne (Poaceae): are fungal endophytes detrimental? American Journal of Botany, 91, 1960-1968.
11. Cheplick G.P., Clay K., Marks S., (1989) Interactions between infection by endophytic fungi and nutrient limitation in the grasses Lolium perenne and Festuca arundinaceae. New Phytologist, 111, 89-97.
12. Christensen M.J., (1996) Antifungal activity in grasses infected with Acremonium and Epichloë endophytes. Australasian Plant Pathology, 25, 186-191.
13. Clarke B.B., White J.F. Jr., Hurley R.H., Torres M.S., Sun S., Huff D.R., (2006) Endophyte mediated suppression of dollar spot disease in fine fescues. Plant Disease, 90, 994-998.
14. Clay K., (1991) Endophytes as antagonists of plant pests. In Microbial Ecology of Leaves, pp. 331-357. Eds, J.H. Andrews, and, S.S. Hirano,. Berlin, Germany: Springer-Verlag.
15. Dixon R.A., (2001) Natural products and plant disease resistance. Nature, 411, 843-847.
16. Eerens J.P.J., Visker M.H.P.W., Lucas R.J., Easton H.S., White J.G.H., (1998) Influence of the ryegrass endophyte (Neotyphodium lolii) in a cool moist environment: IV. Plant parasitic nematodes. New Zealand Journal of Agricultural Research, 41, 209-217.
17. Elliott M.L., (1999) Comparison of Rhizoctonia zeae isolates from Florida and Ohio turfgrasses. HortScience, 34, 298-300.
18. Elmi A.A., West C.P., Robbins R.T., Kirkpatrick T.L., (2000) Endophyte effects on reproduction of root-knot nematode (Meloidogyne marylandi) and osmotic adjustment in tall fescue. Grass Forage Science, 55, 166-172.
19. Farmer E.E., (1985) Effects of fungal elicitor on lignin biosynthesis in cell suspension cultures of soybean. Plant Physiology, 78, 338-342.
20. Ford V.L., Kirkpatrick T.L., (1989) Effects of Acremonium coenophialum in tall fescue on host disease and insect resistance and allelopathy to Pinus taeda seedlings. Arkansas Agricultural Experiment Station Special Report, 140, 29-34.
21. Glenn A.E., Bacon C.W., Price R., Hanlin R.T., (1996) Molecular phylogeny of Acremonium and its taxonomic implications. Mycologia, 88, 369-383.
22. Graham T.L., Graham M.Y., (1996) Signalling in soybean phenylpropanoid responses. Dissection of primary, secondary, and conditioning effects of light, wounding, and elicitor treatments. Plant Physiology, 110, 1123-1133.
23. Gwinn K.D., Gavin A.M., (1992) Relationship between endophyte infestation level of tall fescue seed lots and Rhizoctonia zeae seedling disease. Plant Disease, 76, 911-914.
24. Hamilton C.E., Faeth S.H., (2005) Asexual Neotyphodium endophytes in Arizona fescue: a test of the seed germination and pathogen resistance hypothesis. Symbiosis, 38, 69-85.
25. Hammond-Kosack K.E., Jones J., (1996) Resistance gene-dependent plant defense response. The Plant Cell, 8, 1773-1791.
26. Haygood R.A., Martin S.B., (1990) Characterization and pathogenicity of species of Rhizoctonia associated with centipedegrass and St. Augustinegrass in South Carolina. Plant Disease, 74, 510-514.
27. Johnson M.C., Dahlmann D.L., Siegel M.R., Bush L.P., Latch G.C.M., Potter D.A., Varney D.R., (1985) Insect feeding deterrents in endophyte infected tall fescue. Plant Disease, 70, 380-382.
28. Kolattukudy P.E., (1981) Structure, biosynthesis and biodegradation of cutin and suberin. Annual Review of Plant Physiology, 32, 539-567.
29. Koshino H., Togiya S., Yoshihara T., Sakamura S., (1987) Four fungitoxic C-18 hydroxy unsaturated fatty acids from stromata of Epichloë typhina. Tetrahedron Letters, 28, 73-76.
30. Krauss J., Härri S.A., Bush L., Power S.A., Muller C.B., (2007) Fungal grass endophytes, grass cultivars, nitrogen deposition and the associations with colonizing insects. In Proceedings of the 6th International Symposium on Fungal Endophytes of Grasses, pp. 53-57. Eds A.J. Popay and E.R. Thom. Christchurch, New Zealand, 2006. Dunedin, New Zealand: New Zealand Grassland Association.
31. Lehtonen P.T., Helander M., Siddiqui S.A., Lehto K., Saikkonen K., (2006) Endophytic fungus decreases plant virus infections in meadow ryegrass (Lolium pratense). Biology Letters, 2, 620-623.
32. Lembicz M., Górzyńska K., Leuchtmann A., (2010) Choke disease, caused by Epichloë bromicola, in the grass Agropyron repens in Poland. Plant Disease, 94, 1372.
33. Leuchtmann A., (1992) Systematics, distribution and host specificity of grass endophytes. Natural Toxins, 1, 150-162.
34. Mahmood T., Gergerich R.C., Milus E.A., West C.P., D'Arcy C.J., (1993) Incidence of barley yellow dwarf viruses in wheat, endophyte-infected and endophyte-free tall fescue, and other hosts in Arkansas. Plant Disease, 77, 225-228.
35. Malinowski D., Leuchtmann A., Schmidt D., Nósberger J., (1997) Growth and water status in meadow fescue is affected by Neotyphodium and Phialophora species endophytes. Agronomy Journal, 89, 673-678.
36. Malinowski D.P., Alloush G.A., Belesky D.P., (1998) 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, 1-12.
37. Martin S.B., Lucas L.T., (1984) Characterization and pathogenicity of Rhizoctonia spp. and binucleate Rhizoctonia-like fungi from turfgrasses in North Carolina. Phytopathology, 74, 170-175.
38. Martin S.B., Lucas L.T., Campbell C.L., (1984a) Comparative sensitivity of Rhizoctonia solani and Rhizoctonia-like fungi to selected fungicides in vitro. Phytopathology, 74, 778-781.
39. Martin S.B., Campbell C.L., Lucas L.T., (1984b) Response of Rhizoctonia blights of tall fescue to selected fungicides in the greenhouse. Phytopathology, 74, 782-785.
40. Mauch F., Mauch-Mani B., Boller T., (1988) Antifungal hydrolases in pea tissue II. Inhibition of fungal growth by combinations of chitinase and β-1,3-glucanase. Plant Physiology, 88, 936-942.
41. Mehdy M.C., (1994) Active oxygen species in plant defense against pathogens. Plant Physiology, 105, 467-472.
42. Moy M., Li H.M., Sullivan R., White J.F. Jr., Belanger F.C., (2002) Endophytic fungal β-1,6-gluconase expression in the infected host grass. Plant Physiology, 130, 1298-1308.
43. Nan Z.B., Li C.J., (2001) Neotyphodium in native grasses in China and observations on endophyte/host interactions. In Proceedings of the 4th International Neotyphodium/Grass Interactions Symposium, pp. 41-50. Eds V.H. Paul and P.D. Dapprich. Soest, Germany, 2000a. Soest, Germany: Universität-Gesamthochschule-Paderborn, Abteilung Soest.
44. Pańka D., (2005 a) Infestation of tall fescue (Festuca arundinacea Schreb.) with Neotyphodium coenophialum and its influence on growth of chosen microorganisms in vitro. Acta Agrobotanica, 58, 369-380.
45. Pańka D., (2005 b) Susceptibility of meadow fescue (Festuca pratensis Huds.) infected with endophyte Neotyphodium uncinatum to pathogens. In Recent Advances in Genetics and Breeding of the Grasses, pp. 191-195. Eds, Z. Zwierzykowski, and, A. Kosmala,. Poznań, Poland: Institute of Plant Genetics PAS.
46. Pańka D., (2008) Occurrence of Neotyphodium lolii and its antifungal properties. Phytopathologia Polonica, 48, 5-12.
47. Pańka D., Piesik D., Jeske M., Baturo-Cieśniewska A., (2013) Production of phenolics and the emission of volatile organic compounds by perennial ryegrass (Lolium perenne L.)/Neotyphodium lolii association as a response to infection by Fusarium poae. Journal of Plant Physiology, 170, 1010-1019.
48. Pennell C.G., Ball O.J.-P., (1999) The effects of Neotyphodium endophytes in tall fescue on pasture mealy bug (Balanococcus poae). Proceeding of New Zealand Plant Protection Conference, 52, 259-263.
49. Pennell C.G., Hume D.E., Ball O.J.-P., Easton H.S., Lyons T.B., (2000) Effects of Neotyphodium lolii infection in ryegrass on root aphid and pasture mealy bug. In Proceedings of the 4th International Neotyphodium/Grass Interactions Symposium, pp. 465-469. Eds V.H. Paul and P.D. Dapprich. Soest, Germany, 2000b. Soest, Germany: Universität-Gesamthochschule-Paderborn, Abteilung Soest.
50. Płazek A., Dubas E., (2005) Activation of phenylpropanoid pathway and catalase in leaves of barley and meadow fescue infected by Bipolaris sorokiniania (Sacc.) Shoem. In Recent Advances in Genetics and Breeding of the Grasses, pp. 197-202. Eds, Z. Zwierzykowski, and, A. Kosmala,. Poznań, Poland: Institute of Plant Genetics PAS.
51. Płażek A., Skrzypek E., Żur I., (2000) The change of heat emission and phenolics compounds level in Hordeum vulgare (L.) and Festuca pratensis (Huds.) calli treated with Bipolaris sorokiniana (Sacc.) Schoem. phytotoxins. Journal of Agronomy and Crop Science, 184, 1-72.
52. Popay A.J., Baltus J.G., Pennell C.G., (2000) Insect resistance in perennial ryegrass infected with toxin-free Neotyphodium endophytes. In Proceedings of the 4th International Neotyphodium/Grass Interactions Symposium, pp. 187-193. Eds V.H. Paul and P.D. Dapprich. Soest, Germany, 2000c. Soest, Germany: Universität-Gesamthochschule-Paderborn, Abteilung Soest.
53. Porter J.K., Thompson F.N. Jr., (1992) Effects of fescue toxicosis on reproduction in livestock. Journal of Animal Science, 70, 1594-1603.
54. Powell R.G., Tepaske M.R., Plattner R.D., White J.F., Clement S.L., (1994) Isolation of resveratrol from Festuca versuta and evidence for the widespread occurrence of this stilbene in the Poaceae. Phytochemistry (Oxford), 35, 335-338.
55. Qawasmeh A., Obied H.K., Raman A., Wheatley W., (2012) 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 Agricultural and Food Chemistry, 60, 3381-3388.
56. Rasmussen S., Parsons A.J., Fraser K., Xue K., Newman J.A., (2008) Metabolic profiles of Lolium perenne are differentially affected by nitrogen supply, carbohydrate content, and fungal endophyte infection. Plant Physiology, 146, 1440-1453.
57. Reddy M.N., Faeth S.H., (2010) Damping-off of Festuca arizonica caused by Fusarium. American Journal of Plant Sciences, 1, 104-105.
58. Royals J.K., Martin S.B., Camberato J.J., Jeffers S.N., (2005) Development and evaluation of strategic fungicide programs for control of warm weather diseases in creeping bentgrass. International Turfgrass Society Research Journal, 10, 237-246.
59. Schardl C.L., Leuchtman A., Spiering M.J., (2004) Symbioses of grasses with seedborne fungal endophytes. Annual Review of Plant Biology, 55, 315-340.
60. Schmidt D., (1994) Du nouveau sur les endophytes de la fétuque des prés. Revue Suisse Agriculture, 26, 57-63.
61. Siegel M.R., Bush L.P., (1996) Defensive chemicals in grass-fungal endophyte associations. Recent Advances in Phytochemistry, 30, 81-119.
62. Siegel M.R., Latch G.C., (1991) Expression of antifungal activity in agar culture by isolates of grass endophytes. Mycologia, 83, 529-537.
63. Smiley R.W., Dernoeden P.H., Clarke B.B., (2005) Compendium of Turfgrass Diseases. 3rd edn, pp. 167. St. Paul, MN, USA: APS Press.
64. Smith C.J., (1996) Accumulation of phytoalexins: defense mechanism and stimulus response system. New Phytologist, 132, 1-45.
65. Sneh B., Burpee L., Ogoshi A., (1991) Identification of Rhizoctonia Species, pp. 133. St. Paul, MN, USA: APS Press.
66. Spiers D.E., Evans T.J., Rottinghaus G.E., (2005) Interaction between thermal stress and fescue toxicosis: animal models and new perspectives. In Neotyphodium in Cool-season Grasses, pp. 243-270. Eds, C.A. Roberts, C.P. West, and, D.E. Spiers,. Ames, IA, USA: Blackwell Publishing.
67. Stewart T.M., Mercer C.F., Grant J.L., (1993) Development of meloidogyne nassi on endophyte-infected and endophyte-free perennial ryegrass. Australasian Plant Pathology, 22, 40-41.
68. Tan Y.Y., Spiering M.J., Scott V., Lane G.A., Christensen M.J., Shmid J., (2001) In planta regulation of extension of an endophytic fungus and maintenance of high metabolic rates in its mycelium in the absence of apical extension. Applied and Environmental Microbiology, 67, 5377-5383.
69. Thompson F.N., Stuedeman J.A., (1993) Phytophysiology of fescue toxicosis. Agriculture, Ecosystems and Environment, 44, 263-281.
70. Tian P., Nan Z., Li C., Spangenberg G., (2008) Effect of endophyte Neotyphodium lolii on susceptibility and host physiological response of perennial ryegrass to fungal pathogens. European Journal of Plant Pathology, 122, 593-602.
71. Torres M.S., White J.F., Zhang X., Hinton D.M., Bacon W.C., (2012) Endophyte-mediated adjustments in host morphology and physiology and effects on host fitness traits in grasses. Fungal Ecology, 5, 322-330.
72. Trevathan L.E., (1996) Performance of endophyte-free and endophyte infected tall fescue seedlings in soil infected with Cochliobolus sativus. Canadian Journal of Plant Pathology, 18, 415-418.
73. Vander P., Varum K.M., Domard A., Gueddari N.E.E., Moerschbacher B.M., (1998) Comparison of the ability of partially N-acetylated chitosan and chitooligosaccharides to elicit resistance in wheat leaves. Plant Physiology, 118, 1353-1359.
74. Vincelli P., Powell A.J., (1991) Reaction of perennial ryegrass varieties to red thread, 1990. Biological and Cultural Tests For Control of Plant Diseases, 6, 102.
75. Vranovà E., Inzé D., Van Breusegem F., (2002) Signal transduction during oxidative stress. Journal of Experimental Botany, 53, 1227-1236.
76. Wäli P.R., Helander M., Nissinen O., Saikkonen K., (2006) Susceptibility of endophyte-infected grasses to winter pathogens (snow molds). Canadian Journal of Botany, 84, 1043-1051.
77. Waterhouse A.L., (2001) Determination of total phenolics. In Current Protocols in Food Analytical Chemistry, pp. I1.1.1-I1.1.8. Ed, R.E. Wrolstad,. New York, NY, USA: John Wiley & Sons, Inc.
78. Waterman P.G., Mole S., (1994) Analysis of Phenolic Plant Metabolites, pp. 238 pp. Oxford, UK: Blackwell Scientific Publications.
79. West C.P., (1994) Physiology and drought tolerance of endophyte-infected grasses. In Biotechnology of Endophytic Fungi of Grasses, pp. 87-99. Eds, C.W. Bacon, and, J.F. White, Jr.,. Boca Raton, FL, USA: CRC Press.
80. White J.F. Jr., Cole G.T., (1985) Endophyte host associations in forage grasses III. In vitro inhibition of fungi by Acremonium coenophialum. Mycologia, 77, 487-489.
81. Yue Q., Miller C.J., White J.F., Richardson M.D., (2000) Isolation and characterization of fungal inhibitors from Epichloë festucae. Journal of Agricultural and Food Chemistry, 48, 4687-4692.
82. Zabalgogeazcoa I., Vazquez de Aldana B.R., García Ciudad A., García Criado B., (2003) Fungal endophytes in grasses from semiarid permanent grasslands of Western Spain. Grass and Forage Science, 58, 94-97.
83. Żurek M., Wiewióra B., Żurek G., Prończuk M., (2012) Occurrence of endophyte fungi on grasses in Poland-review. Fungal Ecology, 5, 353-356.