OCCURRENCE OF Neotyphodium AND Epichloë FUNGI IN MEADOW FESCUE AND RED FESCUE IN POLAND AND SCREENING OF ENDOPHYTE ISOLATES AS POTENTIAL BIOLOGICAL CONTROL AGENTS
Dariusz Pańka
University of Technology and Life Sciences in BydgoszczMałgorzata Jeske
University of Technology and Life Sciences in BydgoszczMikołaj Troczyński
University of Technology and Life Sciences in BydgoszczAbstract
Neotyphodium and Epichloë endophytes often influence beneficially on the host plant. Thus, could be used as a biological factor enhancing grass growth and resistance to stress factors. A detailed study was made to: (i) determine the infestation of genotypes of meadow fescue and red fescue, which occur in natural grass communities, in Poland by the Neotyphodium/Epichloë endophytes, (ii) define the level of ergovaline, a toxic alkaloid produced by active associations, (iii) determine the activity of antagonistic distinguishing isolates of endophytic fungi against selected microorganisms. There were analysed 204 genotypes of meadow fescue and 171 genotypes of red fescue. Mean frequency of the infection with endophytes was 74.5% and 64.3% respectively. Ergovaline was produced
by 77% of E+ meadow fescue genotypes and 80.9% of red fescue genotypes. Mean content of the alkaloid was 0.202 and 0.151 μg·g DM-1 respectively. FpII30, FpII67,
FpII77, FpII168 and FrII82 demonstrated a high ability for protection of the host grasses from all the tested pathogens. These isolates due to high antimicrobial activity and a lack of ergovaline production have a great potential for biological control of grasses.
Keywords:
Endophyte, ergovaline, dual-culture, biological controlof grassesReferences
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Bony S., Delatour P., 2001. Revelance and impact of grass endophyte toxins in Europe. In: Proceedings of the 4th International Neotyphodium/Grass Interactions Symposium, V.H. Paul, P.D. Dapprich Soest (eds)., 27-29 September 2000, Universitat-Gesamthochschule Paderborn, Abtailung Soest, Germany, pp. 207-218.
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.
Cagaš B., Flieger M., Olsovska J., 1999. Concentration of ergot alkaloids in Czech ecotypes of Lolium perenne and Festuca pratensis. Grass Forage Sci. 54, 365-370.
Cheplick G.P., Faeth S.H., 2009. Ecology and evolution of the grass-endophyte symbiosis. Oxford, University Press, pp. 241.
Christensen M.J., 1996. Antifungal activity in grasses infected with Acremonium and Epichloë endophytes. Austr. Plant Pathol. 25(3), 186-191.
Clarke B.B., White Jr. J.F., Hurley R.H., Torres M.S., Sun S., Huff D.R., 2006. Endophyte mediated suppresion of dollar spot disease in fine fescues. Plant Dis. 90(8), 994-998.
Dahl Jensen A.M., Mikkelsen L., Roulund N., 2007. Variation in genetic markers and ergovaline production in endophyte (Neotyphodium) – infected fescue species collected in Italy, Spain and Denmark. Crop Sci. 47, 139-147.
Elmi A.A., West C.P., 1995. Endophyte infection effects on stomatal conductance, osmotic adjustment and drought recovery of tall fescue. New Phytol. 131, 61-67.
Elmi A.A., West C.P., Robbins R.T., Kirkpatrik T.L., 2000. Endophyte effects on reproduction of root-knot nematode (Meloidogyne merylandi) and osmotic adjustment in tall fescue. Grass Forage Sci. 55, 166-172.
Faeth S.H., Sullivan T.J., Hamilton C.E., 2001. What maintains high levels of Neotyphodium endophytes in native grasses? A dissecting view and alternative hypotheses. In: Proceedings of the 4th International Neotyphodium/Grass Interactions Symposium, V.H. Paul and P.D. Dapprich (eds.). 2729 September 2000, Universitat-Gesamthochschule Paderborn, Abtailung Soest, Germany, pp. 65-69.
Glenn A.E., Bacon C.W., Price R., Hanlin R.T., 1996. Molecular phylogeny of Acremonium and its taxonomic implications. Mycologia 88, 369-383.
Guillaumin J.J., Frain M., Pichon N., Ravel C., 2001. Survey of fungal endophytes in wild grass species in the Auvergne region (central France). In: Proceedings of the 4th International Neotyphodium/Grass Interactions Symposium,. V.H. Paul and P.D. Dapprich (eds). 27-29 September 2000, Universitat-Gesamthochschule Paderborn, Abtailung Soest, Germany pp. 85-92.
Gundel P.E., Zabalgogeazcoa I., Vázquez de Aldana BR., 2011. Interaction between plant genotype and the symbiosis with Epichloë fungal endophytes in seeds of red fescue (Festuca rubra). Crop Past. Sci. 62(11), 1010-1016.
Gwinn K.D., Gavin A.M., 1992. Relationship between endophyte infestation level of tall fescue seed lots and Rhizoctonia zeae seedling disease. Plant Dis. 76, 911-914.
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 Dis. 70, 380-382.
Kim J.H., Kim C.W., Ahn G.C., Park E.K., Kim C.M., Park K.K., 2007. Ergovaline levels in tall fescue and its effect on performance of lactating cows. Anim. Feed Sci. Tech. 136(3–4), 330-337.
Latch G.C.M., Hunt W.F., Musgrave D.R., 1985. Endophytic fungi affect growth of perennial ryegrass. NZJ Agric. Res. 28, 165-168.
Lembicz M., Górzyńska K., Leuchtmann A., 2010. Choke disease, caused by Epichloë bromicola, in the grass Agropyron repens in Poland. Plant Dis. 94(1), 1372.
Leuchtmann A., 1992. Systematics, distribution and host specificity of grass endophytes. Natural Toxins 1, 150-162.
Lewis G.C., 1994. Incidence of infection of grasses by endophytic fungi in the UK, and effects of infection on animal health, pest and disease damage, and plant growth. IOBC/WPRS Bulletin 17(1), 161-167.
Lewis G.C., 2004. 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. 144, 53-63.
Leyronas C., Raynal G., 2001. Presence of Neotyphodium-like endophytes in European grasses. Ann. App. Biol. 139, 119-129.
Malinowski D.P., Brauer D.K., Belesky D.P., 1999. Neotyphodium coenophialumendophyte affects root morphology of tall fescue grown under phosphorus deficiency. J.
Agron. Crop Sci. 183, 53-60.
Marcinkowska J., 2010. Oznaczanie rodzajów ważnych organizmów fitopatogenicznych (Fungi, Oomycota, Plasmodiophorida). Wyd. SGGW, Warszawa, Poland.
Pańka D., 2005. Infestation of tall fescue (Festuca arundinaceae Schreb.) with Neotyphodium coenophialum and its influence on growth of chosen microorganisms in vitro. Acta Agrobot. 58(2), 369-380.
Pańka D., 2008. Occurrence of Neotyphodium lolii and its antifungal properties Phytopathol. Pol. 48, 5-12.
Pańka D., 2011. Neotyphodium/Epichloë endophytes of perennial ryegrass, meadow fescue and red fescue cultivars cultivated in Poland. Acta Sci. Pol., Hort. Cult. 10(4), 115-131.
Pańka D., Jeske M., Troczyński M., 2011. Effect of Neotyphodium uncinatum endophyte on meadow fescue yielding, health status and ergovaline production in host plants. J. Plant Prot. Res. 51(4), 362-370.
Pańka D., Piesik D., Jeske M., Baturo-Cieśniewska A., 2013a. Production of phenolics and the emission of volatile organic compound (VOCs) by perennial ryegrass (Lolium perenne L.)/Neotyphodium lolii association as a defense reaction against infection by Fusarium poae. J. Plant Physiol (in press).
Pańka D., West C.P., Guerber C.A., Richardson M.D., 2013b. Susceptibility of tall fescue to Rhizoctonia zeae infection as affected by endophyte strain. Ann. Appl. Biol (in press).
Podkówka L., Dorszewski P., Pańka D., 2011. Yield, chemical composition and ensiling ability of green forage from meadow fescue (Festuca pratensis Huds.) infected with Neotyphodium uncinatum. Acta Sci. Pol., Agricultura 10(1), 47-56.
Prończuk M., 2000. Choroby traw – występowanie i szkodliwość w uprawie na nasiona i użytkowaniu trawnikowym. Monografie i Rozprawy Naukowe IHAR-PIB 4, pp. 183.
Reddy M.N., Faeth S.H., 2010. Damping-off of Festuca arizonica caused by Fusarium. Am. J. Plant Sci. 1, 104-105.
Rottinghaus G.E., Garner G.B., Cornell C.N., Ellis J.L., 1991. HPLC method for quantitating ergovaline in endophyte-infested tall fescue: Seasonal variation of ergovaline levels in stems with leaf sheaths, leaf blades, and seedheads. J. Agric. Food Chem. 39, 112-115.
Saha D.C., Jackson M.A., Johnson-Cicalese J.M., 1988. A rapid staining method for detection of endophytic fungi in turf and forage grasses. Phytopathology 78(2), 237-239.
Schardl C.L., 2001. Epicholë festucea and related mutualistic symbionts of grasses. Fung. Gen. Biol. 33, 69-82.
Schmidt D., 1994. Du nouveau sur les endophytes de la fétuque des prés. Revue Suisse Agriculture, 26, 57-63.
Siegel M.R., Schardl C.L., Philips T.D., 1995. Incidence and compatibility of nonclavicipitaceous fungal endophytes in Festuca and Lolium grass species. Mycologia 87(2), 196-202.
Smith S.E., Read D.J., 1997. Mycorrhizal symbiosis. Second edition. Academic Press, San Diego, CA.
Thompson F.N., Stuedeman J.A., 1993. Phytophysiology of fescue toxicosis. Agric. Ecosystems Environ. 44, 263-281.
Vázquez de Aldana BR, García Ciudad A, Zabalgogeazcoa I, García Criado B., 2012. An Epichloë endophyte affects the competitive ability of Festuca rubra against other grassland species. Plant Soil, Doi: 10.1007/s11104-012-1283-7.
Vázquez de Aldana BR, Zabalgogeazcoa I, Rubio de Casas R, García Ciudad A, García Criado B., 2010. Relationships between the genetic distance of Epichloë festucae isolates and the ergovaline and peramine content of their Festuca rubra hosts. Ann. Appl. Biol. 156, 51-61.
Wäli P.R., Helander M., Nissinen O., Saikkonen K., 2006. Susceptibility of endophyte-infected grasses to winter pathogens (snow molds). Can. J. Bot. 84(7), 1043-1051.
Wenzel H., 1948. Zur erfassung des schadenausmasses in pflanzenschutzversuchen. Pflanzenschuzberichte 15, 81-84.
White J.F. Jr., Reddy P.V., 1998. Examination of structure and molecular phylogenetic relationships of some graminicolous symbionts in genera Epichloë and Parepichloë. Mycologia 90, 226-234.
Wiewióra B., 2011. Grzyby endofityczne z rodzaju Neotyphodium występujące w trawach wieloletnich w Polsce oraz ich znaczenie dla upraw pastewnych i trawnikowych. Monografie i Rozprawy Naukowe IHAR-PIB 38, pp. 115.
Zabalgogeazcoa I., Bony S., 2005. Neotyphodium research and application in Europe. In: Neotyphodium in cool-season grasses, Roberts C.A., West C.P., Spiers D.E. (eds).. Blackwell Publ.27-33.
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 Forage Sci. 58, 94-97.
Żurek M., Ochodzki P., Wiewióra B., 2010a. Ocena zawartości ergowaliny w trawach runi wybranych trwałych użytków zielonych na terenie województwa mazowieckiego. Biuletyn IHAR 257/258, 39-47.
Żurek M., Wiewióra B., Żurek G., 2010b. Występowanie grzybów endofitycznych na trwałych użytkach zielonych województwa mazowieckiego. Biuletyn IHAR 256, 171-181.
Żurek M., Wiewióra B., Żurek G., Prończuk M., 2012. Occurrence of endophyte fungi on grasses in Poland – Rev. Fung. Ecol. 5(3), 353-356.
Bony S., Delatour P., 2001. Revelance and impact of grass endophyte toxins in Europe. In: Proceedings of the 4th International Neotyphodium/Grass Interactions Symposium, V.H. Paul, P.D. Dapprich Soest (eds)., 27-29 September 2000, Universitat-Gesamthochschule Paderborn, Abtailung Soest, Germany, pp. 207-218.
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.
Cagaš B., Flieger M., Olsovska J., 1999. Concentration of ergot alkaloids in Czech ecotypes of Lolium perenne and Festuca pratensis. Grass Forage Sci. 54, 365-370.
Cheplick G.P., Faeth S.H., 2009. Ecology and evolution of the grass-endophyte symbiosis. Oxford, University Press, pp. 241.
Christensen M.J., 1996. Antifungal activity in grasses infected with Acremonium and Epichloë endophytes. Austr. Plant Pathol. 25(3), 186-191.
Clarke B.B., White Jr. J.F., Hurley R.H., Torres M.S., Sun S., Huff D.R., 2006. Endophyte mediated suppresion of dollar spot disease in fine fescues. Plant Dis. 90(8), 994-998.
Dahl Jensen A.M., Mikkelsen L., Roulund N., 2007. Variation in genetic markers and ergovaline production in endophyte (Neotyphodium) – infected fescue species collected in Italy, Spain and Denmark. Crop Sci. 47, 139-147.
Elmi A.A., West C.P., 1995. Endophyte infection effects on stomatal conductance, osmotic adjustment and drought recovery of tall fescue. New Phytol. 131, 61-67.
Elmi A.A., West C.P., Robbins R.T., Kirkpatrik T.L., 2000. Endophyte effects on reproduction of root-knot nematode (Meloidogyne merylandi) and osmotic adjustment in tall fescue. Grass Forage Sci. 55, 166-172.
Faeth S.H., Sullivan T.J., Hamilton C.E., 2001. What maintains high levels of Neotyphodium endophytes in native grasses? A dissecting view and alternative hypotheses. In: Proceedings of the 4th International Neotyphodium/Grass Interactions Symposium, V.H. Paul and P.D. Dapprich (eds.). 2729 September 2000, Universitat-Gesamthochschule Paderborn, Abtailung Soest, Germany, pp. 65-69.
Glenn A.E., Bacon C.W., Price R., Hanlin R.T., 1996. Molecular phylogeny of Acremonium and its taxonomic implications. Mycologia 88, 369-383.
Guillaumin J.J., Frain M., Pichon N., Ravel C., 2001. Survey of fungal endophytes in wild grass species in the Auvergne region (central France). In: Proceedings of the 4th International Neotyphodium/Grass Interactions Symposium,. V.H. Paul and P.D. Dapprich (eds). 27-29 September 2000, Universitat-Gesamthochschule Paderborn, Abtailung Soest, Germany pp. 85-92.
Gundel P.E., Zabalgogeazcoa I., Vázquez de Aldana BR., 2011. Interaction between plant genotype and the symbiosis with Epichloë fungal endophytes in seeds of red fescue (Festuca rubra). Crop Past. Sci. 62(11), 1010-1016.
Gwinn K.D., Gavin A.M., 1992. Relationship between endophyte infestation level of tall fescue seed lots and Rhizoctonia zeae seedling disease. Plant Dis. 76, 911-914.
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 Dis. 70, 380-382.
Kim J.H., Kim C.W., Ahn G.C., Park E.K., Kim C.M., Park K.K., 2007. Ergovaline levels in tall fescue and its effect on performance of lactating cows. Anim. Feed Sci. Tech. 136(3–4), 330-337.
Latch G.C.M., Hunt W.F., Musgrave D.R., 1985. Endophytic fungi affect growth of perennial ryegrass. NZJ Agric. Res. 28, 165-168.
Lembicz M., Górzyńska K., Leuchtmann A., 2010. Choke disease, caused by Epichloë bromicola, in the grass Agropyron repens in Poland. Plant Dis. 94(1), 1372.
Leuchtmann A., 1992. Systematics, distribution and host specificity of grass endophytes. Natural Toxins 1, 150-162.
Lewis G.C., 1994. Incidence of infection of grasses by endophytic fungi in the UK, and effects of infection on animal health, pest and disease damage, and plant growth. IOBC/WPRS Bulletin 17(1), 161-167.
Lewis G.C., 2004. 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. 144, 53-63.
Leyronas C., Raynal G., 2001. Presence of Neotyphodium-like endophytes in European grasses. Ann. App. Biol. 139, 119-129.
Malinowski D.P., Brauer D.K., Belesky D.P., 1999. Neotyphodium coenophialumendophyte affects root morphology of tall fescue grown under phosphorus deficiency. J.
Agron. Crop Sci. 183, 53-60.
Marcinkowska J., 2010. Oznaczanie rodzajów ważnych organizmów fitopatogenicznych (Fungi, Oomycota, Plasmodiophorida). Wyd. SGGW, Warszawa, Poland.
Pańka D., 2005. Infestation of tall fescue (Festuca arundinaceae Schreb.) with Neotyphodium coenophialum and its influence on growth of chosen microorganisms in vitro. Acta Agrobot. 58(2), 369-380.
Pańka D., 2008. Occurrence of Neotyphodium lolii and its antifungal properties Phytopathol. Pol. 48, 5-12.
Pańka D., 2011. Neotyphodium/Epichloë endophytes of perennial ryegrass, meadow fescue and red fescue cultivars cultivated in Poland. Acta Sci. Pol., Hort. Cult. 10(4), 115-131.
Pańka D., Jeske M., Troczyński M., 2011. Effect of Neotyphodium uncinatum endophyte on meadow fescue yielding, health status and ergovaline production in host plants. J. Plant Prot. Res. 51(4), 362-370.
Pańka D., Piesik D., Jeske M., Baturo-Cieśniewska A., 2013a. Production of phenolics and the emission of volatile organic compound (VOCs) by perennial ryegrass (Lolium perenne L.)/Neotyphodium lolii association as a defense reaction against infection by Fusarium poae. J. Plant Physiol (in press).
Pańka D., West C.P., Guerber C.A., Richardson M.D., 2013b. Susceptibility of tall fescue to Rhizoctonia zeae infection as affected by endophyte strain. Ann. Appl. Biol (in press).
Podkówka L., Dorszewski P., Pańka D., 2011. Yield, chemical composition and ensiling ability of green forage from meadow fescue (Festuca pratensis Huds.) infected with Neotyphodium uncinatum. Acta Sci. Pol., Agricultura 10(1), 47-56.
Prończuk M., 2000. Choroby traw – występowanie i szkodliwość w uprawie na nasiona i użytkowaniu trawnikowym. Monografie i Rozprawy Naukowe IHAR-PIB 4, pp. 183.
Reddy M.N., Faeth S.H., 2010. Damping-off of Festuca arizonica caused by Fusarium. Am. J. Plant Sci. 1, 104-105.
Rottinghaus G.E., Garner G.B., Cornell C.N., Ellis J.L., 1991. HPLC method for quantitating ergovaline in endophyte-infested tall fescue: Seasonal variation of ergovaline levels in stems with leaf sheaths, leaf blades, and seedheads. J. Agric. Food Chem. 39, 112-115.
Saha D.C., Jackson M.A., Johnson-Cicalese J.M., 1988. A rapid staining method for detection of endophytic fungi in turf and forage grasses. Phytopathology 78(2), 237-239.
Schardl C.L., 2001. Epicholë festucea and related mutualistic symbionts of grasses. Fung. Gen. Biol. 33, 69-82.
Schmidt D., 1994. Du nouveau sur les endophytes de la fétuque des prés. Revue Suisse Agriculture, 26, 57-63.
Siegel M.R., Schardl C.L., Philips T.D., 1995. Incidence and compatibility of nonclavicipitaceous fungal endophytes in Festuca and Lolium grass species. Mycologia 87(2), 196-202.
Smith S.E., Read D.J., 1997. Mycorrhizal symbiosis. Second edition. Academic Press, San Diego, CA.
Thompson F.N., Stuedeman J.A., 1993. Phytophysiology of fescue toxicosis. Agric. Ecosystems Environ. 44, 263-281.
Vázquez de Aldana BR, García Ciudad A, Zabalgogeazcoa I, García Criado B., 2012. An Epichloë endophyte affects the competitive ability of Festuca rubra against other grassland species. Plant Soil, Doi: 10.1007/s11104-012-1283-7.
Vázquez de Aldana BR, Zabalgogeazcoa I, Rubio de Casas R, García Ciudad A, García Criado B., 2010. Relationships between the genetic distance of Epichloë festucae isolates and the ergovaline and peramine content of their Festuca rubra hosts. Ann. Appl. Biol. 156, 51-61.
Wäli P.R., Helander M., Nissinen O., Saikkonen K., 2006. Susceptibility of endophyte-infected grasses to winter pathogens (snow molds). Can. J. Bot. 84(7), 1043-1051.
Wenzel H., 1948. Zur erfassung des schadenausmasses in pflanzenschutzversuchen. Pflanzenschuzberichte 15, 81-84.
White J.F. Jr., Reddy P.V., 1998. Examination of structure and molecular phylogenetic relationships of some graminicolous symbionts in genera Epichloë and Parepichloë. Mycologia 90, 226-234.
Wiewióra B., 2011. Grzyby endofityczne z rodzaju Neotyphodium występujące w trawach wieloletnich w Polsce oraz ich znaczenie dla upraw pastewnych i trawnikowych. Monografie i Rozprawy Naukowe IHAR-PIB 38, pp. 115.
Zabalgogeazcoa I., Bony S., 2005. Neotyphodium research and application in Europe. In: Neotyphodium in cool-season grasses, Roberts C.A., West C.P., Spiers D.E. (eds).. Blackwell Publ.27-33.
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 Forage Sci. 58, 94-97.
Żurek M., Ochodzki P., Wiewióra B., 2010a. Ocena zawartości ergowaliny w trawach runi wybranych trwałych użytków zielonych na terenie województwa mazowieckiego. Biuletyn IHAR 257/258, 39-47.
Żurek M., Wiewióra B., Żurek G., 2010b. Występowanie grzybów endofitycznych na trwałych użytkach zielonych województwa mazowieckiego. Biuletyn IHAR 256, 171-181.
Żurek M., Wiewióra B., Żurek G., Prończuk M., 2012. Occurrence of endophyte fungi on grasses in Poland – Rev. Fung. Ecol. 5(3), 353-356.
Dariusz Pańka
University of Technology and Life Sciences in Bydgoszcz
University of Technology and Life Sciences in Bydgoszcz
Małgorzata Jeske
University of Technology and Life Sciences in Bydgoszcz
University of Technology and Life Sciences in Bydgoszcz
Mikołaj Troczyński
University of Technology and Life Sciences in Bydgoszcz
University of Technology and Life Sciences in Bydgoszcz
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