Advances in research on grass endophytes in agricultural systems and applications in forage breeding

doi:10.11686/cyxb2016049

Abstract

Abstract: The Epichloё endophyte forms mutually beneficial associations with its hosts, which enhance their survival under abiotic and biotic stresses. Modern techniques in molecular biology, genomics, proteomics, metabolomics, and bioinformatics have accelerated research on endophytes. The diversity of secondary metabolites and the genes related to their biosynthesis have been identified and the molecular mechanisms of mutualism between the Epichloё endophyte and its hosts have been clarified. These endophytes are widely utilized in agriculture as they are animal-safe grass endophytes that improve the growth and stress resistance of their hosts, leading to increased pasture persistence, sustainability, and production. Thus, several Epichloё endophytes have been developed and commercialized. In this paper, we review recent research on the interactions between grasses and endophytes, and the effects of endophytes on livestock and on microbial and pasture ecosystems. We also discuss the selection of endophyte strains and forage breeding based on multidisciplinary research.

TIAN Pei, ZHANG Guang-Ming, NAN Zhi-Biao. Advances in research on grass endophytes in agricultural systems and applications in forage breeding[J]. Acta Prataculturae Sinica, 2016, 25(12): 206-220.

References

[1] Nan Z B, Li C J. Roles of the grass- Neotyphodium association in pastoral agriculture systrems. Acta Ecologica Sinica, 2004, 24(3): 605-616.
[2] Bacon C W, Porter J K, Robbins J D, et al . Epichloё typhina from toxic tall fescue grasses. Applied and Environmental Microbiology, 1977, 34(5): 576-581.
[3] Fletcher L R, Harvey I C. An association of a Lolium endophyte with ryegrass staggers. New Zealand Veterinary Journal, 1981, 29(10): 185-186.
[4] Young C A, Hume D E, Mcculley R L. Forages and pastures symposium: Fungal endophytes of tall fescue and perennial ryegrass: Pasture friend or foe. Journal of Animal Science, 2013, 91(5): 2379-2394.
[5] Johnson L J, Bonth A C M, Briggs L R, et al . The exploitation of epichloae endophytes for agricultural benefit. Fungal Diversity, 2013, 60(1): 171-188.
[6] Schardl C L, Young C A, Hesse U, et al . Plant-symbiotic fungi as chemical engineers: multi-genome analysis of the clavicipitaceae reveals dynamics of alkaloid loci. PLoS Genet, 2013, 9(2): e1003323.
[7] Leuchtmann A, Bacon C W, Schardl C L, et al . Nomenclatural realignment of Neotyphodium species with genus Epichloё . Mycologia, 2014, 106(2): 202-215.
[8] Siegel M R, Bush L P. Toxin Production in Grass/Endophyte Associations[M]//Carroll G C, Tudzynski P. The Mycota V. Plant Relationships, Part B. Berlin: Heidelberg Springer, 1997: 185-208.
[9] Bush L P, Wilkinson H H, Schardl C L. Bioprotective alkaloids of grass-fungal endophyte symbioses. Plant Physiology, 1997, 114(1): 1-7.
[10] Prestidge R A. Causes and control of perennial ryegrass staggers in New Zealand. Agriculture, Ecosystems & Environment, 1993, 44(1): 283-300.
[11] Schmidt S P, Osborn T G. Effects of endophyte-infected tall fescue on animal performance. Agriculture, Ecosystems & Environment, 1993, 44(1): 233-262.
[12] Paterson J, Forcherio C, Larson B, et al . The effects of fescue toxicosis on beef cattle productivity. Journal of Animal Science, 1995, 73(3): 889-898.
[13] Faeth S H, Bultman T L. Endophytic Fungi and Interactions Among Host Plants, Herbivores and Natural Enemies[M]//Tscharntke T, Hawkins B A. Multitrophic level interactions. Cambridge: Cambridge University Press, 2002: 89-123.
[14] Clay K, Holah J. Fungal endophyte symbiosis and plant diversity in successional fields. Science, 1999, 285: 1742-1744.
[15] Faeth S H, Sullivan T J. Mutualistic asexual endophytes in a native grass are usually parasitic. The American Naturalist, 2003, 161(2): 310-325.
[16] Latch G C M. Physiological interactions of endophytic fungi and their hosts. Biotic stress tolerance imparted to grasses by endophytes. Agriculture, Ecosystems & Environment, 1993, 44(1): 143-156.
[17] Eerens J P J, Visker M H P W, Lucas R J, et al . Influence of the ryegrass endophyte ( Neotyphodium lolii ) in a cool moist environment. IV. Plant parasitic nematodes. New Zealand Journal of Agricultural Research, 1998, 41(2): 209-217.
[18] Chu-Chou M, Guo B, An Z Q, et al . Suppression of mycorrhizal fungi in fescue by the Acremonium coenophialum endophtyes. Soil Biology and Biochemistry, 1992, 24(7): 633-637.
[19] Guo B Z, Hendrix J, An Z Q, et al . Role of Acremonium endophyte of fescue on inhibition of colonisation and reproduction of mycorrhizal fungi. Mycologia, 1992, 84(6): 882-885.
[20] West C P, Gwinn K D. Role of Acremonium in Drought, Pest, and Disease Tolerance of Grasses[C]//Hume D E. Proceeding of the 2nd International Symposium on Acremonium /Grass Interactions. Palmerstown North: New Zealand Grassland Association, 1993: 3-5.
[21] Nan Z B, Li C J. Neotyphodium in Native Grasses in China and Observations on Endophyte/Host Interactions[C]//Paul V H, Dapprich P D. Proceedings of 4th International Neotyphodium /Grass Interactions Symposium. Soest, 2000: 41-55.
[22] Tian P, Nan Z B, Li C J, et al . 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(4): 593-602.
[23] Ma M Z, Nan Z B. Effect of fungal endophytes against rust disease of perennial ryegrass ( Lolium perenne ) on growth and physiological indices. Acta Prataculturae Sinica, 2011, 20(6): 150-156.
[24] Bacon C W. Abiotic stress tolerances (moisture, nutrients) and photosynthesis in endophyte-infected tall fescue. Agriculture, Ecosystems & Environment, 1993, 44(1): 123-141.
[25] 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(4): 923-940.
[26] Matthews J W, Clay K. Influence of fungal endophyte infection on plant-soil feedback and community interactions. Ecology, 2001, 82(2): 500-509.
[27] Li X Z, Fang A G, Li C J, et al . Advances in the researches on the effects of grass endophytes on other microbes. Acta Ecologica Sinica, 2015, 35(6): 1660-1671.
[28] Wang Z W, Chen Y G, Wang Q C, et al . Progresses and perspectives of studies on plant endophytic microbes in China. Microbiology China, 2014, 41(3): 482-496.
[29] Wang Z W, Ji Y L, Chen Y G. Grass endophytes and their potential applications in agriculture. Journal of Nanjing Agricultural University, 2011, 34(5): 144-154.
[30] Zhang X X, Nan Z B, Li C J. Research progress of improved resistance of the grass to the heavy metal stress by endophyte. Pratacultural Science, 2014, 31(8): 1466-1474.
[31] Kaiser W J, Bruehl G W, Davitt C M, et al . Acremonium isolates from Stipa robusta . Mycologia, 1996, 88(4): 539-547.
[32] Li C J, Nan Z B, Volker H P, et al . A new Neotyphodium species symbiotic with drunken horse grass ( Achnatherum inebrians ) in China. Mycotaxon, 2004, 90(1): 141-147.
[33] Ji Y L, Zhan L H, Kang Y, et al . A new stromata-producing Neotyphodium species symbiotic with clonal grass Calamagrostis epigeios (L.) Roth. grown in China. Mycologia, 2009, 101(2): 200-205.
[34] Chen L, Li X Z, Li C J, et al . Two distinct Epichloё species symbiotic with Achnatherum inebrians , drunken horse grass. Mycologia, 2015, 107(4): 15-19.
[35] Jin W J, Li C J, Wang Z F. Research advances on diversity of grass Epichloё endophytes. Acta Prataculturae Sinica, 2015, 24(1): 168-175.
[36] Faeth S H, Helander M L, Saikkonen K T. Asexual Neotyphodium endophytes in a native grass reduce competitive abilities. Ecology Letters, 2004, 7(4): 304-313.
[37] Tibbets T M, Faeth S H. Neotyphodium endophytes in grasses: deterrents or promoters of herbivory by leaf-cutting ants. Oecologia, 1999, 118(3): 297-305.
[38] Cheplick G P, Perera A, Koulouris K. Effect of drought on the growth of Lolium perenne genotypes with and without fungal endophytes. Functional Ecology, 2000, 14(6): 657-667.
[39] Cheplick G P. Recovery from drought stress in Lolium perenne (Poaceae): are fungal endophytes detrimental. American Journal of Botany, 2004, 91(12): 1960-1968.
[40] Jia T, Ren A Z, Wei M Y, et al . Effects of endophyte transmission on ecophysiological characteristics of Achnatherum sibiricum . Chinese Journal of Plant Ecology, 2015, 39(1): 72-80.
[41] Hoveland C S. Importance and economic significance of the Acremonium endophytes to performance of animals and grass plant. Agriculture, Ecosystems & Environment, 1993, 44(1): 3-12.
[42] Joost R E. Acremonium in fescue and ryegrass: boon or bane? A review. Journal of Animal Science, 1995, 73(3): 881-888.
[43] Schardl C L, Leuchtmann A, Spiering M J. Symbioses of grasses with seedborne fungal endophytes. Annual Review of Plant Biology, 2004, 55: 315-340.
[44] Siegel M R, Latch G C, Johnson M C. Fungal endophytes of grasses. Annual Review of Phytopathology, 1987, 25(1): 293-315.
[45] Li C J, Nan Z B, Zhang C J, et al . Effects of drunken horse grass infected with endophyte on Chinese rabbit. Journal of Agricultural Science and Technology, 2009, 11(2): 90.
[46] Mackintosh C G, Orr M B, Gallagher R T, et al . Ryegrass staggers in Canadian Wapiti deer. New Zealand Veterinary Journal, 1982, 30(7): 106-107.
[47] Alabdouli K, Blythe L, Duringer J, et al . Physiological effects of endophyte-infected perennial ryegrass straw on female camels in the Middle East. Emirates Journal of Food and Agriculture, 2014, 26(1): 82-92.
[48] Reed K, Vaughan J, Cummins L, et al . Impact of mycotoxins and of a mycotoxin deactivator on alpacas grazing perennial ryegrass infected with wild endophyte ( Neotyphodium spp.). Animal Production Science, 2010, 50(9): 902-908.
[49] Browning R. Effect of the wild-type tall fescue endophyte on growth rate and feed consumption in nulliparous meat goat does. Small Ruminant Research, 2012, 105(1): 29-32.
[50] Di Menna M, Finch S, Popay A, et al . A review of the Neotyphodium lolii / Lolium perenne symbiosis and its associated effects on animal and plant health, with particular emphasis on ryegrass staggers. New Zealand Veterinary Journal, 2012, 60(6): 315-328.
[51] Prestidge R A, Pottinger R P, Barker G M. An Association of Lolium Endophyte with Ryegrass Resistance to Argentine Stem Weevil[C]//New Zealand Weed and Pest Control Society. Proceedings of the 35th New Zealand Weed and Pest Control Conference. Hamilton, New Zealand, 1982: 199-222.
[52] Ball O J P, Christensen M J, Prestidge R A. Effect of Selected Isolates of Acremonium Endophytes on Adult Black Beetle ( Heteronychus arator ) Feeding[C]//New Zealand Plant Pretection Society. Proceedings of the New Zealand Plant Protection Conference. New Zealand: Waitangi, 1994: 227.
[53] Porter J K. Analysis of endophyte toxins: fescue and other grasses toxic to livestock. Journal of Animal Science, 1995, 73(3): 871-880.
[54] Richmond D S, Kunkel B A, Somasekhar N, et al . Top-down and bottom-up regulation of herbivores: Spodoptera frugiperda turns tables on endophyte-mediated plant defence and virulence of an entomopathogenic nematode. Ecological Entomology, 2004, 29(3): 353-360.
[55] Tapper B A, Lane G A. Janthitrems Found in a Neotyphodium Endophyte of Perennial Ryegrass[C]//Kallenbach R, Rosenkrans C F, Lock T R. 5th International Symposium on Neotyphodium /Grass Interactions. Arkansas: Fayetteville, 2004: 301.
[56] Popay A J, Gerard P J. Cultivar and Endophyte effects on a root aphid, Aploneura lentisci , in perennial ryegrass. New Zealand Plant Protection, 2007, 60: 223-227.
[57] Fuchs B, Krischke M, Mueller M J, et al . Peramine and lolitrem b from endophyte-grass associations cascade up the food chain. Journal of Chemical Ecology, 2013, 39(11/12): 1385-1389.
[58] Omacini M, Chaneton E J, Ghersa C M, et al . Symbiotic fungal endophytes control insect host-parasite interaction webs. Nature, 2001, 409: 78-81.
[59] Li T, Blande J D, Gundel P E, et al . Epichloё endophytes alter inducible indirect defences in host grasses. Plos One, 2014, 9(6): e101331.
[60] Bultman T L, Rodstrom J L, Radabaugh K R, et al . Influence of genetic variation in the fungal endophyte of a grass on an herbivore and its parasitoid. Entomologia Experimentalis et Applicata, 2009, 130(2): 173-180.
[61] Bultman T L, Mcneill M R, Goldson S L. Isolate-dependent impacts of fungal endophytes in a multitrophic interaction. Oikos, 2003, 102(3): 491-496.
[62] Richmond D S, Bigelow C A. Variation in endophyte-plant associations influence black cutworm (lepidoptera: noctuidae) performance and susceptibility to the parasitic nematode Steinernema carpocapsae . Environmental Entomology, 2009, 38(4): 996-1004.
[63] Miyazaki S, Ikeda T, Hanazumi M, et al . Toxicological Evaluation of Endophyte-infected Perennial Ryegrass Straw to Japanese Black Steers[C]//Proceedings of the 6th International Symposium on Fungal Endophytes of Grasses. Christchurch, New Zealand: New Zealand Grassland Association, 2007: 415-418.
[64] Finch S, Thom E, Babu J, et al . The evaluation of fungal endophyte toxin residues in milk. New Zealand Veterinary Journal, 2013, 61(1): 11-17.
[65] Finch S, Fletcher L, Babu J. The evaluation of endophyte toxin residues in sheep fat. New Zealand Veterinary Journal, 2012, 60(1): 56-60.
[66] Tian P. Interactions of Ryegrass, Neotyphodium lolii and Several Plant Pathogenic Fungi[D]. Lanzhou: Lanzhou University, 2009.
[67] Bacon C W, Richardson M D, White J F. Modification and uses of endophyte-enhanced turfgrasses: a role for molecular technology. Crop Science, 1997, 37(37): 1415-1425.
[68] Lewis G C. Effect of cutting height on perennial ryegrass with and without infection with endophyte and ryegrass mosaic virus. Iobc Wprs Bulletin, 1996, 19: 55-58.
[69] Guy P L, Davis L T. Variation in the incidence of Barley yellow dwarf virus and in the ability of Neotyphodium endophytes to deter feeding by aphids ( Rhopalosiphum padi ) on Australasian tall fescue. Australasian Plant Pathology, 2002, 31(3): 307-308.
[70] Márquez L M, Redman R S, Rodriguez R J, et al . A virus in a fungus in a plant: three-way symbiosis required for thermal tolerance. Science, 2007, 315: 513-515.
[71] Herrero N, Márquez S S, Zabalgogeazcoa I. Mycoviruses are common among different species of endophytic fungi of grasses. Archives of Virology, 2009, 154(2): 327-330.
[72] Romo M, Leuchtmann A, García B, et al . A totivirus infecting the mutualistic fungal endophyte Epichloё festucae . Virus Research, 2007, 124(1): 38-43.
[73] Marulanda A, Azcon R, Ruiz-Lozano J M. Contribution of six arbuscular mycorrhizal fungal isolates to water uptake by Lactuca sativa plants under drought stress. Physiologia Plantarum, 2003, 119(4): 526-533.
[74] Yang G W, Liu N, Yang X, et al . Relationship between arbuscular mycorrhizal fungi and individual plant and their effects on plant productivity and species diversity of plant community. Acta Prataculturae Sinica, 2015, 24(6): 188-203.
[75] Müller J. Artificial infection by endophytes affects growth and mycorrhizal colonisation of Lolium perenne . Functional Plant Biology, 2003, 30(4): 419-424.
[76] Novas M V, Iannone L J, Godeas A M, et al . Evidence for leaf endophyte regulation of root symbionts: effect of Neotyphodium endophytes on the pre-infective state of mycorrhizal fungi. Symbiosis, 2011, 55(1): 19-28.
[77] Larimer A L, Bever J D, Clay K. The interactive effects of plant microbial symbionts: a review and meta-analysis. Symbiosis, 2010, 51(2): 139-148.
[78] Liu Q H, Parsons A J, Xue H, et al . Competition between foliar Neotyphodium lolii endophytes and mycorrhizal Glomus spp. fungi in Lolium perenne depends on resource supply and host carbohydrate content. Functional Ecology, 2011, 25(4): 910-920.
[79] Vicari M, Hatcher P E, Ayres P G. Combined effect of foliar and mycorrhizal endophytes on an insect herbivore. Ecology, 2002, 83(9): 2452-2464.
[80] Mcnear D H Jr, Mcculley R L. Influence of the Neotyphodium ——Tall fescue symbiosis on belowground processes. Plant and Soil Sciences Faculty Publications, 2012, http: //uknowledge.uky.edu/pss_facpub/44.
[81] Casas C, Omacini M, Montecchia M S, et al . Soil microbial community responses to the fungal endophyte Neotyphodium in Italian ryegrass. Plant and Soil, 2011, 340(1/2): 347-355.
[82] Iqbal J, Siegrist J A, Nelson J A, et al . Fungal endophyte infection increases carbon sequestration potential of southeastern USA tall fescue stands. Soil Biology and Biochemistry, 2012, 44(1): 81-92.
[83] Roberts E L, Ferraro A. Rhizosphere microbiome selection by Epichloё endophytes of Festuca arundinacea . Plant and Soil, 2015, 396(1/2): 229-239.
[84] Nourbakhsh F, Abbasi S, Mirlohi A, et al . Endophyte ( Epichloё coenophiala ) symbiosis increased enzyme activities in the rhizosphere of tall fescue under greenhouse condition. Advances in Environmental Biology, 2014, 8(22): 380-384.
[85] Van Hecke M M, Treonis A M, Kaufman J R. How does the fungal endophyte Neotyphodium coenophialum affect tall fescue ( Festuca arundinacea ) rhizodeposition and soil microorganisms. Plant and Soil, 2005, 275(1/2): 101-109.
[86] Franzluebbers A, Stuedemann J. Soil carbon and nitrogen pools in response to tall fescue endophyte infection, fertilization, and cultivar. Soil Science Society of America Journal, 2005, 69(2): 396-403.
[87] Rudgers J A, Clay K. Endophyte symbiosis with tall fescue: how strong are the impacts on communities and ecosystems. Fungal Biology Reviews, 2007, 21(2): 107-124.
[88] Saikkonen K, Gundel P, Helander M. Chemical ecology mediated by fungal endophytes in grasses. Journal of Chemical Ecology, 2013, 39(7): 962-968.
[89] Coley A B, Fribourg H A, Pelton M R, et al . Effects of tall fescue endophyte infestation on relative abundance of small mammals. Journal of Environmental Quality, 1995, 24(3): 472-475.
[90] Rudgers J A, Clay K. An invasive plant-fungal mutualism reduces arthropod diversity. Ecology Letters, 2008, 11(8): 831-840.
[91] Yao X, Christensen M J, Bao G, et al . A toxic endophyte-infected grass helps reverse degradation and loss of biodiversity of over-grazed grasslands in northwest China. Scientific Reports, 2015, 5: 18527.
[92] Guo J, Mcculley R L, Mcnear Jr D H. Tall fescue cultivar and fungal endophyte combinations influence plant growth and root exudate composition. Frontiers in Plant Science, 2015, 6: 183.
[93] Wakelin S, Harrison S, Mander C, et al . Impacts of endophyte infection of ryegrass on rhizosphere metabolome and microbial community. Crop and Pasture Science, 2015, 66(10): 1049-1057.
[94] Iqbal J, Nelson J A, Mcculley R L. Fungal endophyte presence and genotype affect plant diversity and soil-to-atmosphere trace gas fluxes. Plant and Soil, 2013, 364(1/2): 15-27.
[95] Mcculley R L. Does Aboveground Fungal Endophyte Genotype Similarly Affect Belowground Arbuscular Mycorrhizal Fungal Colonization of Tall Fescue Roots and Associated Plant and Soil Parameters[C]//9th International Symposium on Fungal Endophytes of Grasses and 1st International Symposium on Plant Microbiomes. Australian: Melbourne, 2015: 52.
[96] Rasmussen S, Parsons A, Newman J A. Metabolomics analysis of the Lolium perenne — Neotyphodium lolii symbiosis: more than just alkaloids. Phytochemistry Reviews, 2009, 8(3): 535-550.
[97] Schardl C L, Young C A, Faulkner J R, et al . Chemotypic diversity of epichloae, fungal symbionts of grasses. Fungal Ecology, 2012, 5(3): 331-344.
[98] Ekanayake P, Rabinovich M, Guthridge K, et al . Phylogenomics of fescue grass-derived fungal endophytes based on selected nuclear genes and the mitochondrial gene complement. BMC Evolutionary Biology, 2013, 13: 270.
[99] Hettiarachchige I K, Ekanayake P N, Mann R C, et al . Phylogenomics of asexual Epichloё fungal endophytes forming associations with perennial ryegrass. BMC Evolutionary Biology, 2015, 15: 72.
[100] Van Zijll De Jong E, Dobrowolski M P, Sandford A, et al . Detection and characterisation of novel fungal endophyte genotypic variation in cultivars of perennial ryegrass ( Lolium perenne L.). Australian Journal of Agricultural Research, 2008, 59(3): 214-221.
[101] Van Zijll De Jong E, Dobrowolski M P, Bannan N, et al . Global genetic diversity of the perennial ryegrass fungal endophyte Neotyphodium lolii . Crop Science, 2008, 48(4): 1487-1501.
[102] Charlton N D, Shoji J Y, Ghimire S R, et al . Deletion of the fungal gene soft disrupts mutualistic symbiosis between the grass endophyte epichloё festucae and the host plant. Eukaryotic Cell, 2012, 11(12): 1463-1471.
[103] Panaccione D G, Johnson R D, Wang J, et al . 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, 2001, 98(22): 12820-12825.
[104] Young C A, Felitti S, Shields K, et al . A complex gene cluster for indole-diterpene biosynthesis in the grass endophyte Neotyphodium lolii . Fungal Genet Biology, 2006, 43(10): 679-693.
[105] Fleetwood D J, Scott B, Lane G A, et al . A complex ergovaline gene cluster in Epichloё endophytes of grasses. Applied and Enviromental Microbiology, 2007, 73(8): 2571-2579.
[106] Young C A, Tapper B A, May K, et al . Indole-diterpene biosynthetic capability of Epichloё endophytes as predicted by ltm gene analysis. Applied and Environmental Microbiology, 2009, 75(7): 2200-2211.
[107] Takach J E, Mittal S, Swoboda G A, et al . Genotypic and chemotypic diversity of Neotyphodium endophytes in tall fescue from greece. Applied and Environmental Microbiology, 2012, 78(16): 5501-5510.
[108] Charlton N D, Craven K D, Afkhami M E, et al . Interspecific hybridization and bioactive alkaloid variation increases diversity in endophytic Epichloё species of Bromus laevipes . FEMS Microbiology Ecology, 2014, 90(1): 276-289.
[109] Pan J, Bhardwaj M, Faulkner J R, et al . Ether bridge formation in loline alkaloid biosynthesis. Phytochemistry, 2014, 98: 60-68.
[110] Felitti S, Shields K, Ramsperger M, et al . Transcriptome analysis of Neotyphodium and Epichloё grass endophytes. Fungal Genetics and Biology, 2006, 43(7): 465-475.
[111] Dinkins R D, Barnes A, Waters W. Microarray analysis of endophyte-infected and endophyte-free tall fescue. Journal of Plant Physiology, 2010, 167(14): 1197-1203.
[112] Johnson L J, Johnson R D, Schardl C L, et al . Identification of differentially expressed genes in the mutualistic association of tall fescue with Neotyphodium coenophialum . Physiological and Molecular Plant Pathology, 2003, 63(6): 305-317.
[113] Eaton C J, Cox M P, Ambrose B, et al . Disruption of signaling in a fungal-grass symbiosis leads to pathogenesis. Plant Physiology, 2010, 153(4): 1780-1794.
[114] Eaton C J, Dupont P Y, Solomon P, et al . A core gene set describes the molecular basis of mutualism and antagonism in Epichloё spp. Molecular Plant-Microbe Interactions, 2015, 28(3): 218-231.
[115] Dupont P Y, Eaton C J, Wargent J J, et al . Fungal endophyte infection of ryegrass reprograms host metabolism and alters development. New Phytologist, 2015, 208(4): 1227-1240.
[116] Tanaka A, Christensen M J, Takemoto D, et al . Reactive oxygen species play a role in regulating a fungus-perennial ryegrass mutualistic interaction. Plant Cell, 2006, 18(4): 1052-1066.
[117] Tanaka A, Takemoto D, Hyon G S, et al . NoxA activation by the small GTPase RacA is required to maintain a mutualistic symbiotic association between Epichloё festucae and perennial ryegrass. Molecular Microbiology, 2008, 68(5): 1165-1178.
[118] Takemoto D, Tanaka A, Kayano Y, et al . Reactive Oxygen as a Signal in Grass- Epichloё Symbiosis[C]//Young C A, Aiken G E, McCulley R L, et al . Epichloae, Endophytes of Cool Season Grasses: Implications, Utilization and Biology. Proceedings of the 7th International Symposium on Fungal Endophytes of Grasses. USA: Lexington, Kentucky, 2012: 109-112.
[119] Scott B, Eaton C J. Role of reactive oxygen species in fungal cellular differentiations. Current Opinion in Microbiology, 2008, 11(6): 488-493.
[120] Tanaka A, Cartwright G M, Saikia S, et al . ProA, a transcriptional regulator of fungal fruiting body development, regulates leaf hyphal network development in the Epichloё festucae - Lolium perenne symbiosis. Molecular Microbiology, 2013, 90(3): 551-568.
[121] Koulman A, Lee T V, Fraser K, et al . Identification of extracellular siderophores and a related peptide from the endophytic fungus Epichloё festucae in culture and endophyte-infected Lolium perenne . Phytochemistry, 2012, 75: 128-139.
[122] Rasmussen S, Parsons A J, Fraser K, et al . Metabolic profiles of Lolium perenne are differentially affected by nitrogen supply, carbohydrate content, and fungal endophyte infection. Plant Physiology, 2008, 146(3): 1440-1453.
[123] Nagabhyru P, Dinkins R D, Wood C L, et al . Tall fescue endophyte effects on tolerance to water-deficit stress. BMC Plant Biology, 2013, 13: 127.
[124] Zhou L Y. Physio-Biochemical Mechanism of Festuca sinensis — Epichloё Symbiossis Exposure to Cold Stress[D]. Lanzhou: Lanzhou University, 2015.
[125] Lehner A F, Craig M, Fannin N, et al . Electrospray[+] tandem quadrupole mass spectrometry in the elucidation of ergot alkaloids chromatographed by HPLC: screening of grass or forage samples for novel toxic compounds. Journal of Mass Spectrometry, 2005, 40(11): 1484-1502.
[126] Browning R, Leite-Browning M L. Effect of ergotamine and ergonovine on thermal regulation and cardiovascular function in cattle. Journal of Animal Science, 1997, 75(1): 176-181.
[127] Larson B T, Harmon D L, Piper E L, et al . Alkaloid binding and activation of D 2 dopamine receptors in cell culture. Journal of Animal Science, 1999, 77(4): 942-947.
[128] Moubarak A S, Johnson Z B, Rosenkrans Jr C F. Antagonistic effects of simultaneous exposure of ergot alkaloids on kidney adenosine triphosphatase system. In Vitro Cellular & Developmental Biology-Animal, 2003, 39(8/9): 395-398.
[129] Guerre P. Ergot alkaloids produced by endophytic fungi of the genus Epichloё . Toxins, 2015, 7(3): 773-790.
[130] De Battista J P, Bouton J H, Bacon C W, et al . Rhizome and herbage production of endophyte-removed tall fescue clones and populations. Agronomy Journal, 1990, 82(4): 651-654.
[131] Koshino H, Yoshihara T, Ichihara A, et al . Two sphingoid derivatives from stromata of Epichloe typhin A on Phleum pratense . Phytochemistry, 1992, 31(11): 3757-3759.
[132] Niones J T, Takemoto D. An isolate of Epichloё festucae , an endophytic fungus of temperate grasses, has growth inhibitory activity against selected grass pathogens. Journal of General Plant Pathology, 2014, 80(4): 337-347.
[133] Song Q Y, Nan Z B, Gao K, et al . Antifungal, phytotoxic, and cytotoxic activities of metabolites from Epichloё bromicola , a fungus obtained from Elymus tangutorum grass. Journal of Agricultural and Food Chemistry, 2015, 63(40): 8787-8792.
[134] Fletcher L R. Managin Ryegrass-Endophyte Toxicoses[M]//Roberts C A, West C P, Spiers D E. Neotyphodium in Cool-Season Grasses. Blackwell, 2005: 229-241.
[135] Reed K F M, Nie Z N, Walker L V, et al . Fluctuations in the concentration of ergovaline and lolitrem B produced by the wild-type endophyte ( Neotyphodium lolii ) in perennial ryegrass ( Lolium perenne ) pasture. Animal Production Science, 2011, 51(12): 1098-1108.
[136] Hunt M G, Newman J A. Reduced herbivore resistance from a novel grass-endophyte association. Journal of Applied Ecology, 2005, 42(4): 762-769.
[137] Milne G. Technology Transfer of Novel Ryegrass Endophytes in New Zealand[C]//Proceedings 6th International Symposium on Fungal Endophytes of Grasses. New Zealand, Christchurch: Grassland Research and Practice Series, 2007: 237-239.
[138] Kaur J, Ekanayake P, Tian P, et al . Discovery and characterisation of novel asexual Epichloё endophytes from perennial ryegrass ( Lolium perenne L.). Crop and Pasture Science, 2015, 66(10): 1058-1070.
[139] Gunter S A, Beck P A. Novel endophyte-infected tall fescue for growing beef cattle. Journal of Animal Science, 2004, 82(13_suppl): 75-82.
[140] Pennell C G L, Rolston M P. Novel Uses of Grass Endophyte Technology[C]//The 8 th International Symposium on Fungal Endophyte of Grasses. Lanzhou, 2012: 211-214.
[141] Fletcher L. “Non-toxic” endophytes in ryegrass and their effect on livestock health and production. Ryegrass endophyte: an essential New Zealand symbiosis. Grassland Research and Practice Series, 1999, 7: 133-139.
[142] Popay A, Marshall S, Baltus J. Endophyte infection influences disappearance of perennial ryegrass seed. New Zealand Plant Protection, 2000, 23: 398-405.
[143] Bluett S J, Thom E R, Clark D A, et al . Effects of perennial ryegrass infected with either AR1 or wild endophyte on dairy production in the Waikato. New Zealand Journal of Agricultural Research, 2005, 48(2): 197-212.
[144] Jensen J G, Popay A J. Perennial ryegrass infected with AR37 endophyte reduces survival of porina larvae. New Zealand Plant Protection, 2004, 57: 323.
[145] Hume D E, Popay A J, Cooper B M, et al . Effect of a Novel Endophyte on the Productivity of Perennial Ryegrass ( Lolium perenne ) in New Zealand[C]//5th International Symposium on Neotyphodium /Grass Interactions. USA: Fayetteville, Arkansas, Poster, 2004.
[146] Edwards G R, Bryant R H. What Perennial Ryegrass Should You Sow[C]//South Island Dairy Event (SIDE) Conference. Canterbury: Lincoln University, 2011: 27-29.
[147] Popay A J, Hume D E, Mainland R A, et al . Field resistance to Argentine stem weevil ( Listronotus bonariensis ) in different ryegrass cultivars infected with an endophyte deficient in lolitrem B. New Zealand Journal of Agricultural Research, 1995, 38(4): 519-528.
[148] Nihsen M E, Piper E L, West C P, et al . Growth rate and physiology of steers grazing tall fescue inoculated with novel endophytes. Journal of Animal Science, 2004, 82(3): 878-883.
[149] Tapper B A, Latch G C M. Selection Against Toxin Production in Endophyte-infected Perennial Ryegrass[C]//Woodfield D R, Mattews C. Ryegrass Endophyte: An Essential New Zealand Symbiosis. Napier, New Zealand: New Zealand Grassland Association, 1999: 107-111.
[150] Popay A J, Hume D E, Davis K L, et al . Interactions between endophyte ( Neotyphodium spp.) and ploidy in hybrid and perennial ryegrass cultivars and their effects on Argentine stem weevil ( Listronotus bonariensis ). New Zealand Journal of Agricultural Research, 2003, 46(4): 311-319.
[151] Simpson W R, Faville M J, Moraga R A, et al . Epichloё fungal endophytes and the formation of synthetic symbioses in Hordeeae (=Triticeae) grasses. Journal of Systematics and Evolution, 2014, 52: 794-806.
[1] 南志标, 李春杰. 禾草内生真菌共生体在草地农业系统中的作用. 生态学报, 2004, 24(3): 605-616.
[23] 马敏芝, 南志标. 内生真菌对感染锈病黑麦草生长和生理的影响. 草业学报, 2011, 20(6): 150-156.
[27] 李秀璋, 方爱国, 李春杰, 等. 禾草内生真菌对其它微生物的影响研究进展. 生态学报, 2015, 35(6): 1660-1671.
[28] 王志伟, 陈永敢, 王庆璨, 等. 中国植物内生微生物研究的发展和展望. 微生物学通报, 2014, 41(3): 482-496.
[29] 王志伟, 纪燕玲, 陈永敢. 禾本科植物内生真菌及其在农业上的应用潜力. 南京农业大学学报, 2011, 34(5): 144-154.
[30] 张兴旭, 南志标, 李春杰. 内生真菌提高禾草耐重金属胁迫的研究进展. 草业科学, 2014, 31(8): 1466-1474.
[35] 金文进, 李春杰, 王正凤. 禾草内生真菌的多样性及意义. 草业学报, 2015, 24(1): 168-175.
[40] 贾彤, 任安芝, 魏茂英, 等. 不同传播方式的内生真菌感染对羽茅的生理生态影响. 植物生态学报, 2015, 39(1): 72-80.
[45] 李春杰, 南志标, 张昌吉, 等. 醉马草内生真菌对家兔的影响. 中国农业科技导报, 2009, 11(2): 90.
[66] 田沛. 多年生黑麦草, 内生真菌与数种植物病原真菌的互作[D]. 兰州: 兰州大学, 2009.
[74] 杨高文, 刘楠, 杨鑫, 等. 丛枝菌根真菌与个体植物的关系及其对群落生产力和物种多样性的影响. 草业学报, 2015, 24(6): 188-203.
[124] 周连玉. 基于代谢组学的中华羊茅-内生真菌共生体响应低温胁迫的生化机制[D]. 兰州: 兰州大学, 2015.