Chin J Plan Ecolo ›› 2015, Vol. 39 ›› Issue (6): 621-634.doi: 10.17521/cjpe.2015.0060

• Orginal Article • Previous Articles     Next Articles

Potential analysis of grass endophytes Neotyphodium as biocontrol agents

LI Xiu-Zhang, YAO Xiang, LI Chun-Jie*(), NAN Zhi-Biao   

  1. State Key Laboratory of Grassland Agro-ecosystems;College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou 730020, China
  • Received:2014-11-14 Accepted:2015-05-20 Online:2015-07-02 Published:2015-06-01
  • Contact: Chun-Jie LI
  • About author:

    # Co-first authors


Many grasses in the subfamily Pooideae develop symbioses with Neotyphodium fungal endophytes, which exist widely in nature. The stably symbiotic relationship not only ensures accessible nutrients required by Neotyphodium fungal endophytes, but also significantly increases the resistance of host grasses to biological stresses through the production of secondary metabolites. Previous studies show that infected grasses with endophytic fungi have prominently enhanced resistance to pests, plant diseases, companion plants and other biological stresses. Grass endophytic fungi show remarkable resistant to at least 79 species of pests from three classes; arachnida, nematode and insecta, and to at least 22 species of pathogenic fungi. Although the biotechnological application of endophytic fungi in grass breeding for variety selection and quality improvement has progressed well, opportunities remain for further exploring the use of fungal endophytes among different host grasses coupled with the examination of genetic stability of Neotyphodium in novel host grasses. In the future application of endophytic fungi as a bio-control method, researchers should not only consider specificities of host grasses, but also need to have comprehensive analysis and knowledge about the mutual relationships among grasses, endophytic fungi and ecological environments, which will help use endophytic fungi to better serve humanity.

Key words: Neotyphodium, pest resistance, disease resistance, biocontrol factor, potential analysis

Table 1

Insect, nematodes and mites deterred by Neotyphodium/Epichloë species (adapted from Kuldau & Bacon, 2008)"

内生真菌 Endophyte 宿主植物 Host plant 害虫 Pest
Epichloë glyceriae 苇状羊茅 Festuca arundinacea 禾谷缢管蚜 Rhopalosiphum padi
E. sylvatica 短柄草 Brachypodium sylvaticum 草地贪夜蛾 Spodoptera frugiperda
E. festucae 苇状羊茅 F. arundinacea Endria inimica
东亚飞蝗 Locusta migratoria
黑腹果蝇 Drosophila melanogaster
Exitianus exitiosus
麦长管蚜 Sitobion avenae
紫羊茅 F. rubra Meloidogyne naasi
Metopolophium festucae
Meloidogyne marylandii
Anguina funina
帽状纽带线虫 Hoplolaimus galeatus
双角螺旋线虫 Helicotylenchus digonicus
异毛刺线虫属 Paratrichodorus sp.
E. festuca var. lolii 多花黑麦草 Lolium perenne 黑异爪蔗金龟 Heteronychus arator
E. typhina 苇状羊茅 F. arundinacea Balanococcus poae
Graphania mutans
Persectania ewingii
Neotyphodium coenophialum 苇状羊茅 F. arundinacea 草螟蛾属 Crambus sp.
赤拟谷盗 Tribolium castaneum
Exomala orientalis
玉米跳甲 Chaetocnema pulicaria
禾谷缢管蚜 Rhopalosiphum padi
黑角负泥虫 Oulema melanopus
Adoryphorus coulonii
Graphania mutans
Prosapia bicincta
玉米螟 Ostrinia nubilalis
日本丽金龟 Popillia japonica
乳香平翅根蚜 Aploneura lentisci
斯克里布纳短体线虫 Pratylenchus scribneri
白符跳 Folsomia candida
咖啡短体线虫 Pratylenchus goodeyi
Sphenophorus inaequalis
玉米蚜 Rhopalosiphum maidis
Pogonomyrmex rugosus
N. gansuense 醉马草 Achnatherum inebrians 猬草瘿螨 Abacarus hystrix
亚洲小车蝗 Oedaleus decorus
针毛收获蚁 Messor aciculatus
Pogonomyrmex rugosus
罗格斯石竹蚁 Tetranychus cinnabarinus
N. uncinatum 草甸羊茅 F. pratensis 阿根廷茎象甲 Listronotus bonariensis
玉米跳甲 Chaetocnema pulicaria
黑异爪蔗金龟 Heteronychus arator
褐新西兰肋翅鳃角金龟 Costelytra zealandica
内生真菌 Endophyte 宿主植物 Host plant 害虫 Pest
短齿默林线虫 Merlinius brevidens
伤残短体线虫 Pratylenchus pratensis
索氏短体线虫 Pratylenchus thornei
原始毛刺线虫 Trichodorus primitivus
早熟禾缢瘤蚜 Rhopalomyzus poae
N. lolii 多花黑麦草 L. perenne 澳洲日野黑蟋蟀 Teleogryllus commodus
Parapediasia sp.
Meloidogyne naasi
大螟 Sesamia inferens
Cyclocephala lurida
Meloidogyne marylandii
玉米跳甲 Chaetocnema pulicaria
谷物锈螨 Abacarus hystrix
禾谷缢管蚜 Rhopalosiphum padi
黑角负泥虫 Oulema melanopus
Draeculocephala cephala
家蟋蟀 Acheta domesticus
麦无网长管蚜 Metopolophium dirhodum
Graphania mutans
玉米螟 Ostrinia nubilalis
乳香平翅根蚜 Aploneura lentisci
条沙叶蝉Psammotettix striatus
Bitylenchus maximus
Bitylenchus dubius
亚洲玉米螟 Ostrinia furnacalis
Agallia constricta
玉米蚜 Rhopalosiphum maidis
N. starrii 亚利桑那羊茅 F. arizonica 黄地老虎 Agrotis segetum
小地老虎 Agrotis ipsilon
Agrotis infusa
Neotyphodium spp. 布顿大麦草 Hordeum bogdanii 麦双尾蚜 Diuraphis noxia
草甸羊茅 F. pratensis 美洲毛谷杆长蝽 Blissus leucopterus hirtus
苇状羊茅 F. arundinacea Philobota productella
Cyclocephala lurida
玉米跳甲 Chaetocnema pulicaria
Aphodius tasmaniae
黄伪毛蚜 Sipha flava
褐新西兰肋翅鳃角金龟 Costelytra zealandica
麦二叉蚜 Schizaphis graminum
Draeculacephala antica
Sphenophorus minimus
杂拟谷盗 Tribolium confusum
多花黑麦草 L. perenne 阿根廷茎象甲 Listronotus bonariensis
滨海油葫芦 Teleogryllus oceanicus
莓蚜 Sitobion fragariae
内生真菌 Endophyte 宿主植物 Host plant 害虫 Pest
长毛草盲蝽 Lygus rugulipennis
玉米跳甲 Chaetocnema pulicaria
Mythimna convecta
Graminella nigrifrons
锯谷盗 Oryzaephilus surinamensis
赤须盲蝽 Trigonotylus caelestialium
Sphenophorus venatus
麦二叉蚜 Schizaphis graminum
乳草长蝽 Oncopeltus fasciatus
Persectania ewingii
Trigonotylus caelestialum
较小拟毛刺线虫 Paratrichodorus minor
Mythimna unipuncta
早熟禾结网毛虫 Parapediasia teterrella
牧草尖隐喙象 Sphenophorus parvulus
粘虫 Mythimna separate
Pseudalectia unipunctata
野大麦 H. brevisubulatum subsp. violaceum 麦双尾蚜 Diuraphis noxia
紫羊茅 F. rubra 美洲毛谷杆长蝽 Blissus leucopterus hirtus
[1] Antunes PM, Miller J, Carvalho LM, Klironomos JN, Newman JA (2008). Even after death the endophytic fungus of Schedonorus phoenix reduces the arbuscular mycorrhizas of other plants.Functional Ecology, 22, 912-918.
[2] Bacetty AA, Snook ME, Glenn AE, Noe JP, Hill N, Culbreath A, Timper P, Nagabhyru P, Bacon CW (2009). Toxicity of endophyte-infected tall fescue alkaloids and grass metabolites on Pratylenchus scribneri.Phytopathology, 99, 1336-1345.
[3] Bacon CW, Lyons PC, Porter JK, Robbins JD (1986). Ergot toxicity from endophyte-infected grasses: A review.Agronomy Journal, 78, 106-116.
[4] Ball OJP, Prestidge RA, Sprosen JM (1995). Interrelationships between Acremonium lolii, peramine, and lolitrem B in perennial ryegrass.Applied and Environmental Micro- biology, 61, 1527-1533.
[5] Barratt BIP, Crook KE, Ferguson CM, Johnstone PD, Malone LA (2008). Developing a method for laboratory biosafety testing impacts of transgenic plants on non-target insects.Entomologia Experimentalis et Applicata, 128, 437-449.
[6] Barrientos-Lozano L, Hernández-Velázquez VR, Milner RJ, Hunter DM (2002). Advances in biological control of locusts and grasshoppers in Mexico.Journal of Orthoptera Research, 11, 77-82.
[7] Belovsky GE, Slade JB (1995). Dynamics of two Montana grasshopper populations: Relationships among weather, food abundance and intraspecific competition.Oecologia, 101, 383-396.
[8] Blank CA (1992). Interactions of Tall Fescue Seedlings Infected with Acremonium coenophialum with Soilborne Pathogens. Master degree dissertation, University of Tennessee, Knoxville.
[9] Blankenship JD, Spiering MJ, Wilkinson HH, Fannin FF, Bush LP, Schardl CL (2001). Production of loline alkaloids by the grass endophyte, Neotyphodium uncinatum, in defined media.Phytochemistry, 58, 395-401.
[10] Bouton J, Easton S (2005). Endophytes in forage cultivars. In: Roberts CA, West CP, Spiers DE eds. Neotyphodium in Cool-Season Grasses. Blackwell Publishing, Oxford, UK. 325-340.
[11] Breen JP (1993). Enhanced resistance to fall armyworm (Lepidoptera: Noctudiae) in Acremonium endophyte infected turfgrasses.Journal of Economic Entomology, 86, 621-629.
[12] Brem D, Leuchtmann A (2002). Intraspecific competition of endophyte infected vs uninfected plants of two woodland grass species.Oikos, 96, 281-290.
[13] Brundrett MC (2009). Mycorrhizal associations and other means of nutrition of vascular plants: Understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis.Plant and Soil, 320, 37-77.
[14] Bryant RH, Cameron NE, Edwards GR (2010). Response of black beetle and red-headed pasture cockchafer larvae to loline alkaloids in meadow fescue roots.New Zealand Plant Protection, 63, 219-223.
[15] Bultman TJ, Bell G, Martin WD (2004). A fungal endophyte mediates reversal of wound-induced resistance and constrains tolerance in a grass.Ecology, 85, 679-685.
[16] Bultman TL, Rodstrom JL, Radabaugh KR, VanDop JD, Librizzi JM, Longwell LL, Pulas C, Grant L, Sullivan TJ (2009). Influence of genetic variation in the fungal endophyte of a grass on an herbivore and its parasitoid.Entomologia Experimentalis et Applicata, 130, 173-180.
[17] Bush LP, Wilkinson HH, Schardl CL (1997). Bioprotective alkaloids of grass-fungal endophyte symbioses.Plant Physiology, 114, 1-7.
[18] Cheplick GP, Clay K (1988). Acquired chemical defences in grasses: The role of fungal endophytes.Oikis, 52, 309-318.
[19] Christensen MJ, Latch GCM (1991). Variation among isolates of Acremonium endophytes (A. coenophialum and possibly A. typhinum) from tall fescue (Festuca arundinacea).Mycological Research, 95, 1123-1126.
[20] Clarke BB, White JF, Hurley RH, Torres MS, Sun S, Huff DF (2006). Endophyte-mediated suppression of dollar spot disease in fine fescues.Plant Disease, 90, 994-998.
[21] Clay K (1990). Fungal endophytes of grasses.Annual Review of Ecology Systematics, 21, 275-297.
[22] Clay K, Hardy TN, Hammond AM Jr (1985). Fungal endophytes of grasses and their effects on an insect herbivore.Oecologia, 66, 1-5.
[23] Clay K, Holah J (1999). Fungal endophyte symbiosis and plant diversity in successional fields.Science, 285, 1742-1744.
[24] Clay K, Holah J, Rudgers JA, Moran NA (2005). Herbivores cause a rapid increase in hereditary symbiosis and alter plant community composition.Proceedings of the National Academy of Sciences of the United States of America, 102, 12465-12470.
[25] Clay K, Schardl C (2002). Evolutionary origins and ecological consequences of endophyte symbiosis with grasses.The American Naturalist, 160, S99-S127.
[26] Clement SL, Elberson LR (2010). Variable effects of grass-Neotyphodium associations on cereal leaf beetle (Coleoptera: Chrysomelidae) feeding, development and survival.Journal of Entomological Science, 45, 197-203.
[27] Clement SL, Hu JG, Stewart AV, Wang B, Elberson LR (2011). Detrimental and neutral effects of a wild grass-fungal endophyte symbiotum on insect preference and performance.Journal of Insect Science, 11, 77.
[28] Conover MR (2003). Impact of the consumption of endophyte-infected perennial ryegrass by meadow voles.Agriculture Ecosystems & Environment, 97, 199-203.
[29] Cross DL, Redmond LM, Strickland JR (1995). Equine fescue toxicosis: Signs and solutions.Journal of Animal Science, 73, 899-908.
[30] Cunningham IJ (1958). Non-toxicity to animals of ryegrass endophyte and other endophytic fungi of New Zealand grasses.New Zealand Journal of Agricultural Research, 1, 489-497.
[31] de Sassi C, Müller CB, Krauss J (2006). Fungal plant endosymbionts alter life history and reproductive success of aphid predators.Proceedings of the Royal Society B: Biological Sciences, 273, 1301-1306.
[32] Dugan FM, Sitton JW, Sullivan RF, White JFJ (2002). The Neotyphodium endophyte of wild barley (Hordeum brevisubulatum subsp. violaceum) grows and sporulates on leaf surfaces of the host.Symbiosis, 32, 147-159.
[33] Easton HS (2007). Grasses and Neotyphodium endophytes: Co-adaptation and adaptive breeding.Euphytica, 154, 295-306.
[34] Eaton CJ, Cox MP, Ambrose B, Becker M, Hesse U, Schardl CL, Scott B (2010). Disruption of signaling in a fungal-grass symbiosis leads to pathogenesis.Plant Physiology, 153, 1780-1794.
[35] Elmi AA, West CP, Robbins RT, Kirkpatrick TL (2000). Endophyte effects on reproduction of a root-knot nematode (Meloidogyne marylandi) and osmotic adjustment in tall fescue.Grass and Forage Science, 55, 166-172.
[36] Engle JS, Madden LV, Lipps PE (2003). Evaluation of inoculation methods to determine resistance reactions of wheat to Fusarium graminearum.Plant Disease, 87, 1530-1535.
[37] Faeth SH (2002). Are endophytic fungi defensive plant mutualists?Oikos, 98, 25-36.
[38] Franzluebbers AJ, Hill NS (2005). Soil carbon, nitrogen, and ergot alkaloids with short- and long-term exposure to endophyte-infected and endophyte-free tall fescue.Soil Science Society of America Journal, 69, 404-412.
[39] Franzluebbers AJ, Nazih N, Stuedemann JA, Fuhrmann JJ, Schomberg HH, Hartel PG (1999). Soil carbon and nitrogen pools under low- and high-endophyte-infected tall fescue.Soil Science Society of America Journal, 63, 1687-1694.
[40] Funk CR, White RH, Breen JP (1993). Importance of Acremonium endophytes in turf-grass breeding and management.Agriculture Ecosystems & Environment, 44, 215-232.
[41] Gao JH, Nan ZB (2007). A review of bioprotective alkaloids of grass-fungal endophyte symbioses.Acta Ecologica Sinica, 27, 2531-2546. (in Chinese with English abstract)
[高嘉卉, 南志标 (2007). 禾草内生真菌生物碱的研究进展. 生态学报, 27, 2531-2546.]
[42] Greulich F, Horio E, Shimanuki T, Yoshihara T (1999). Field results confirm natural plant protection by the endophytic fungus Epichloë typhina against the pathogenic fungus Cladosporium phlei on timothy leaves.Japanese Journal of Phytopathology, 65, 454-459.
[43] Gwinn KD, Gavin AM (1992). Relationship between endophyte infestation level of tall fescue seed lots and Rhizoctonia zeae seedling disease.Plant Disease, 76, 911-914.
[44] Hoveland CS, Schmidt SP, King CCJ, Odom JW, Clark EM, McGuire JA, Smith LA, Grimes HW, Holliman JL (1983). Steer performance and association of Acremonium coenophialum fungal endophyte on tall fescue pasture.Agronomy Journal, 75, 821-824.
[45] Huang X, Li CJ, Nan ZB, Yang S, Chai Q (2010). Effect of Achnatherum inebrians infected with Neotyphodium endophyte on accompanying species of Stipa capillata and Poa sphondylodes.Acta Prataculturae Sinica, 19(5), 87-93. (in Chinese with English abstract)
[黄玺, 李春杰, 南志标, 杨松, 柴青 (2010). 醉马草内生真菌对其伴生种硬质早熟禾和针茅生长的影响. 草业学报, 19(5), 87-93.]
[46] Jia T, Ren AZ, Wei MY, Yin LJ, Gao YB (2015). Effect of endophyte transmission on ecophysiological character- istics of Achnatherum sibiricum.Chinese Journal of Plant Ecology, 39, 72-80. (in Chinese with English abstract)
[贾彤, 任安芝, 魏茂英, 尹立佳, 高玉葆 (2015). 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, 39, 72-80.]
[47] Johnson MC, Bush LP, Siegel MR (1986). Infection of tall fescue with Acremonium coenophialum by means of callus culture.Plant Diseases, 70, 380-382.
[48] Johnson-Cicalese JM, White RH (1990). Effect of Acremonium endophytes on four species of billbug found on New Jersey turfgrasses.Journal of The American Society for Horticultural Science, 115, 602-604.
[49] Kasai E, Sasaki T, Okazaki H (2004). Artificial infection of Italian ryegrass (Lolium multiflorum Lam.) with Neotyph- odium uncinatum.Japanese Society of Grassland Science, 50, 180-186.
[50] Kimmons CA, Gwinn KD, Bernard EC (1990). Nematode reproduction on endophyte-infected and endophyte-free tall fescue.Plant Disease, 74, 757-761.
[51] Kuldau G, Bacon C (2008). Clavicipitaceous endophytes: Their ability to enhance resistance of grasses to multiple stresses.Biological Control, 46, 57-71.
[52] Kunkel BA, Grewal PS, Quigley MF (2004). A mechanism of acquired resistance against an entomopathogenic nematode by Agrotis ipsilon feeding on perennial ryegrass harboring a fungal endophyte.Biological Control, 29, 100-108.
[53] Latch GCM (1993). Physiological interactions of endophytic fungi and their hosts. Biotic stress tolerance imparted to grasses by endophytes.Agriculture Ecosystems & Environment, 44, 143-156.
[54] Latch GCM, Christensen MJ, Gaynor DL (1985). Aphid detection of endophyte infection in tall fescue.New Zealand Journal of Agricultural Research, 28, 129-132.
[55] Leuchtmann A, Bacon CW, Schardl CL, White JF Jr, Tadych M (2014). Nomenclatural realignment of Neotyphodium species with genus Epichloë.Mycologia, 106, 202-215.
[56] Lewandowski SM, Bushnell WR, Evans CK (2006). Distribu- tion of mycelial colonies and lesions in field-grown barley inoculated with Fusarium graminearum.Phytopathology, 96, 567-581.
[57] Li CJ, Gao JH, Nan ZB (2007a). Interactions of Neotyphodium gansuense, Achnatherum inebrians, and plant-pathogenic fungi.Mycological Research, 111, 1220-1227.
[58] Li CJ, Nan ZB, Paul VH, Dapprich PD, Liu Y (2004). A new Neotyphodium species symbiotic with drunken horse grass (Achnatherum inebrians) in China.Mycotaxon, 90, 141-147.
[59] Li CJ, Zhang XX, Li F, Nan ZB, Schardl L (2007b). Disease and pest resistance of endophyte infected and non-infected drunken horse grass. In: Popay A, Thom ER eds. Proceedings of the 6th International Symposium on Fungal Endophytes of Grasses. New Zealand Grassland Association, Dunedin, New Zealand. 111-114.
[60] Li XZ, Fang AG, Li CJ, Nan ZB (2015). Advances in the researches on the effects of grass endophytes on other microbes.Acta Ecologica Sinica, 35, 1660-1671. (in Chinese with English abstract)
[李秀璋, 方爱国, 李春杰, 南志标 (2015). 禾草内生真菌对其他微生物的影响研究进展. 生态学报, 35, 1660-1671.]
[61] Ma MZ, Nan ZB (2011). Effect of fungal endophytes against rust disease of perennial rygrass (Lolium perenne) on growth and physiological indices.Acta Prataculturae Sinica, 20(6), 150-156. (in Chinese with English abstract)
[马敏芝, 南志标 (2011).内生真菌对感染锈病黑麦草生长和生理的影响. 草业学报, 20(6), 150-156.]
[62] Mack KML, Rudgers JA (2008). Balancing multiple mutualists: Asymmetric interactions among plants, arbuscular mycorrhizal fungi, and fungal endophytes.Oikos, 117, 310-320.
[63] Mahmood T, Gergerich RC, Milus EA, West CP, D’arcy CJ (1993). Barley yellow dwarf viruses in wheat, endophyte-infected and endophyte-free tall fescue, and other hosts in Arkansas.Plant Disease, 77, 225-228.
[64] Malinowski DP, Alloush GA, Belesky DP (2000). Leaf endophyte Neotyphodium coenophialum modifies mineral uptake in tall fescue.Plant and Soil, 227, 115-126.
[65] Malinowski DP, Belesky DP (2006). Ecological importance of Neotyphodium spp. grass endophytes in agroecosystems.Grassland Science, 52, 1-14.
[66] Malinowski DP, Belesky DP, Fedders JM (1999a). Endophyte infection may affect the competitive ability of tall fescue grown with red clover.Journal of Agronomy and Crop Science, 183, 91-101.
[67] Malinowski DP, Brauer DK, Belesky DP (1999b). The endophyte Neotyphodium coenophialum affects root morphology of tall fescue grown under phosphorus deficiency.Journal of Agronomy and Crop Science, 183, 53-60.
[68] Malinowski DP, Leuchtmann A, Schmidt D, Nösberger J (1997). Growth and water status in meadow fescue is affected by Neotyphodium and Phialophora species endophytes.Agronomy Journal, 89, 673-678.
[69] Mortimer PH, Di Menna ME (1983). Ryegrass staggers: Further substantiation of a Lolium endophyte aetiology and the discovery of weevil resistance of ryegrass pastures infected with Loloum endophyte.Proceedings New Zealand Gressland Association, 44, 240-243.
[70] Moy M, Belanger F, Duncan R, Freehoff A, Leary C, Meyer W, Sullivan R, White JF Jr (2000). Identification of epiphyllous mycelial nets on leaves of grasses infected by clavicipitaceous endophytes.Symbiosis, 28, 291-302.
[71] Murray FR, Latch GCM, Scott DB (1992). Surrogate transformation of perennial ryegrass, Lolium perenne, using genetically modified Acremonium endophyte.Molecular and General Genetics MGC, 233, 1-9.
[72] Nan ZB, Li CJ (2000). Neotyphodium in native grasses in China and observations on endophyte/hosts interactions. In: Roberts CA, West CP, Spiers DA eds. Neotyphodium in Cool-season Grasses. Blackwell Publishing, Ames, Iowa. 163-185.
[73] Nan ZB, Li CJ (2004). Roles of the grass-Neotyphodium association in pastoral agriculture systems.Acta Ecologica Sinica, 24, 605-616. (in Chinese with English abstract)
[南志标, 李春杰 (2004). 禾草内生真菌共生体在草地农业系统中的作用. 生态学报, 24, 605-616.]
[74] Omacini M, Chaneton EJ, Ghersa CM, Müller CB (2001). Symbiotic fungal endophytes control insect host-parasite interaction webs.Nature, 409, 78-81.
[75] Panaccione DG, Kotcon JB, Schardl CL, Johnson RD, Morton JB (2006). Ergot alkaloids are not essential for endophytic fungus-associated population suppression of the lesion nematode, Pratylenchus scribneri, on perennial ryegrass.Nematology, 8, 583-590.
[76] Pańka D, Podkówka L, Lamparski R (2004). Preliminary observations on the resistance of meadow fescue (Festuca pratensis Huds.) infected by Neotyphodium uncinatum to diseases and pest and nutritive value. In: Kallenbach R, Rosenkrans CF Jr, Lock TR eds. Proceedings 5th International Symposium on Neotyphodium/Grass Interac- tions, May 23-26, 2004. University of Arkansas, Fayet- teville, USA.
[77] Pennell CGL, Rolston MP, de Bonth A, Simpson WR, Hume DE (2010). Development of a bird-deterrent fungal endophyte in turf tall fescue.New Zealand Journal of Agricultural Research, 53, 145-150.
[78] Popay AJ, Bonos SA (2005). Biotic responses in endophytic grasses. In: Roberts CA, West CP, Spiers DE eds. Neotyphodium in Cool-season Grasses. Blackwell Publishing, Oxford, UK.
[79] Porras-Alfaro A, Bayman P (2011). Hidden fungi, emergent properties: Endophytes and microbiomes.Annual Review of Phytopatholology, 49, 291-315.
[80] Potter DA, Patterson CG, Redmond CT (1992). Influence of turfgrass species and tall fescue endophyte on feeding ecology of Japanese beetle and southern masked chafer grabs (Coeloptera: Scarabaeidae).Journal of Economic Entomology, 85, 900-909.
[81] Prestidge RA, Gallagher RT (1988). Endophyte fungus confers resistance to ryegrass: Argentine stem weevil larval studies.Ecological Entomology, 13, 429-435.
[82] Prestidge RA, Pottinger RP, Barker GM (1982). An association of Lolium endophyte with ryegrass resistance to Argentine stem weevil―Proceedings of the 35th New Zealand weed and pest control conference.New Zealand Plant Protection Society, 35, 199-222.
[83] Rasmussen S, Parsons AJ, Poppy A, Xue H, Newman JA (2008). Plant-endophyte-herbivore interactions: More than just alkaloids?Plant Signaling & Behavior, 3, 974-977.
[84] Ren AZ, Clay K (2009). Impact of a horizontally transmitted endophyte, Balansia henningsiana, on growth and drought tolerance of Panicum rigidulum.International Journal of Plant Sciences, 170, 599-608.
[85] Richmond DS, Kunkel BA, Somasekhar N, Grewal PS (2004). Top-down and bottom-up regulation of herbivores: Spodoptera frugiperda turns the tables on endophyte- mediated plant defence and virulence of an entom- opathogenic nematode.Ecological Entomology, 29, 353-360.
[86] Roberts CA, West CP, Spiers DE (2008). Neotyphodium in Cool-season Grasses. 2nd edn. Blackwell Publishing, Oxford, UK.
[87] Rodriguez RJ, White JF, Arnold AE, Redman RS (2009). Fungal endophytes: Diversity and functional roles.New Phytologist, 182, 314-330.
[88] Rowan DD, Hunt MB, Gaynor DL (1986). Peramine, a novel insect feeding deterrent from ryegrass infected with the endophyte Acremonium loliae.Journal of the Chemical Society, Chemical Communications, 12, 935-936.
[89] Rowan DD, Latch GCM (1994). Utilization of endophyte- infected perennial ryegrasses for increased insect resistance. In: Bacon CW, White JF Jr eds. Biotechnology of Endophytic Fungi of Grasses. CRC Press, Boca Raton, USA.
[90] Rudgers JA, Clay K (2008). An invasive plant-fungal mutu- alism reduces arthropod diversity.Ecology Letters, 11, 831-840.
[91] Rudgers JA, Koslow JM, Clay K (2004). Endophytic fungi alter relationships between diversity and ecosystem properties.Ecology Letters, 7, 42-51.
[92] Salminen SO, Richmond DS, Grewal SK, Grewal PS (2005). Influence of temperature on alkaloid levels and fall armyworm performance in endophytic tall fescue and perennial ryegrass.Entomologia Experimentalis et Applicata, 115, 417-426.
[93] Schardl CL (2001). Epichloë festucae and related mutualistic symbionts of grasses.Fungal Genetics and Biology, 33, 69-82.
[94] Schardl CL (2009). Fungal endophytes in Lolium and Festuca species. In: Schardl CL ed. Molecular Breeding of Forage and Turf. Springer, New York. 285-298.
[95] Schardl CL (2010). The Epichloë, symbionts of the grass subfamily Poöideae.Annals of the Missouri Botanical Garden, 97, 646-665.
[96] Schardl CL, Grossman RB, Nagabhyru P, Faulkner JR, Mallik UP (2007). Loline alkaloids: Currencies of mutualism.Phytochemistry, 68, 980-996.
[97] Schardl CL, Leuchtmann A, Spiering MJ (2004). Symbioses of grasses with seedborne fungal endophytes.Annual Review of Plant Biology, 55, 315-340.
[98] Schardl CL, Panaccione DG, Tudzynski P (2006). Ergot alkaloids―biology and molecular biology.The alkaloids Chemistry and Biology, 63, 45-86.
[99] Schardl CL, Young CA, Pan J, Florea S, Takach JE, Panaccione DG, Farman ML, Webb JS, Jaromczyk J, Charlton ND, Nagabhyru P, Chen L, Shi C, Leuchtmann A (2013). Currencies of mutualisms: Sources of alkaloid genes in vertically transmitted epichloae.Toxins, 5, 1064-1088.
[100] Schmidt SP, Oshorn TG (1993). Effects of endophyte-infected tall fescue on animal performance.Agriculture Ecosystems & Environment, 44, 232-262.
[101] Scott B, Schardl C (1993). Fungal symbionts of grasses: Evolutionary insights and agricultural potential.Trends in Microbiology, 1, 196-200.
[102] Shiba T, Sasaki T, Kasai E (2007). Resistance to the rice leaf bug (Trigonotylus caelestialium) is conferred by Neotyphodium endophyte infection of Italian ryegrass (Lolium multiflorum).Japanese Society of Grassland Science, 53, 205-209.
[103] Shiba T, Sugawara K (2010). Inhibitory effect of an endophytic fungus, Neotyphodium lolii, on the feeding and survival of Ostrinia furnacalis (Guenee) (Lepidoptera: Pyralidae) and Sesamia inferens (Walker) (Lepidoptera: Noctuidae) on infected Lolium perenne.Applied Entomology and Zoology, 45, 225-231.
[104] Shiba T, Sugawara K, Arakawa A (2011). Evaluating the fungal endophyte Neotyphodium occultans for resistance to the rice leaf bug, Trigonotylus caelestialium, in Italian ryegrass, Lolium multiflorum.Entomologia Experimentalis et Applicata, 141, 45-51.
[105] Siegel MR (1993). Acremonium endophytes: Our current state of knowledge and future directions for research.Agriculture, Ecosystems & Environment, 44, 301-321.
[106] Siegel MR, Latch GCM, Bush LP, Fannin FF, Rowan DD, Tapper BA, Bacon CW, Johnson MC (1990). Fungal endophyte-infected grasses: Alkaloid accumulation and aphid response.Journal of Chemical Ecology, 16, 3301-3315.
[107] Siegel MR, Latch GCM, Johnson MC (1987). Fungal endophytes of grasses.Annual Review of Phytopathology, 25, 293-315.
[108] Strobel G, Daisy B (2003). Bioprospecting for microbial endophytes and their natural products.Microbiology and Molecular Biology Reviews, 67, 491-502.
[109] Stuedemann JA, Hoveland CS (1988). Fescue endophyte: History and impact on animal agriculture.Journal of Production Agriculture, 1, 39-44.
[110] Sutherland BL, Hume DE, Tapper BA (1999). Allelopathic effects of endophyte-infected perennial ryegrass extracts on white clover seedlings.New Zealand Journal of Agricultural Research, 42, 19-26.
[111] Tadych M, Bergen M, Dugan FM, White JF Jr (2007). Evaluation of the potential role of water in spread of conidia of the Neotyphodium endophyte of Poa ampla.Mycological Research, 111, 466-472.
[112] Takemoto D, Kamakura S, Saikia S, Becker Y, Wrenn R, Tanaka A, Sumimoto H, Scott B (2011). Polarity proteins Bem1 and Cdc24 are components of the filamentous fungal NADPH oxidase complex.Proceedings of the National Academy of Sciences of the United States of America, 108, 2861-2866.
[113] Tanaka A, Takemoto D, Hyon GS, Park P, Scott B (2008). NoxA activation by the small GTPase RacA is required to maintain a mutualistic symbiotic association between Epichloë festucae and perennial ryegrass.Molecular Microbiology, 68, 1165-1178.
[114] Tanaka A, Tapper BA, Popay A, Parker EJ, Scott B (2005). A symbiosis expressed non-ribosomal peptide synthetase from a mutualistic fungal endophyte of perennial ryegrass confers protection to the symbiotum from insect herbivory.Molecular Microbiolgy, 57, 1036-1050.
[115] Tapper BA, Lane GA (2004). Janthitrems found in a Neo- typhodium endophyte of perennial ryegrass. In: Kallenbach R, Rosenkranz CJ, Lock TR eds. 5th International Symposium on Neotyphodium. University of Arkansa, Fayetteville, USA.
[116] Tian P, Nan ZB, Li CJ, Spangenberg G (2008). Effect of the endophyte Neotyphodium lolii on susceptibility and host physiological response of perennial ryegrass to fungal pathogens.European Journal of Plant Pathology, 122, 593-602.
[117] Vázquez-de-Aldana BR, Zabalgogeazcoa I, García-Ciudad A, García-Criado B (2013). An Epichloë endophyte affects the competitive ability of Festuca rubra against other grassland species.Plant and Soil, 362, 201-213.
[118] Wang ZY, Jiang SP (2007). Effect of Endophytic fungi on defensive enzymes activity of tall fescue leaves.Journal of Anhui Agricultural Sciences, 35, 361-362. (in Chinese with English abstract)
[王志勇, 江淑平 (2007). 内生真菌对高羊茅叶内防御酶活性的影响. 安徽农业科学, 35, 361-362.]
[119] Wei YK, Gao YB (2008). Review of the diversity of endophyte genetics and symbiotic interactions with grasses.Chinese Journal of Plant Ecology, 32, 512-520. (in Chinese with English abstract)
[魏宇昆, 高玉葆 (2008). 禾草内生真菌的遗传多样性及其共生关系. 植物生态学报, 32, 512-520.]
[120] White JF Jr (1988). Endophyte-host associations in forage grasses. XI. A proposal concerning origin and evolution.Mycologia, 80, 442-446.
[121] White JF Jr, Martin TI, Cabral D (1996). Endophyte-host associations in grasses. XXII. Conidia formation by Acremonium endophytes on the phylloplanes of Agrostis hiemalis and Poa rigidifolia. Mycologia, 88, 174-178.
[122] White JF Jr, Morgan-Jones G (1987). Endophyte-host associations in forages. VII. Acremonium chisosum, a new species isolated from Stipa eminens in Texas.Mycotaxon, 28, 179-189.
[123] White JF Jr, Torres MS (2010). Is plant endophyte-mediated defensive mutualism the result of oxidative stress protection?Physiologia Plantarum, 138, 440-446.
[124] Wilson D (1995). Endophyte―The evolution of a term, and clarification of its use and definition.Oikos, 73, 274-276.
[125] Xu R, Nan ZB, Zhou YF, Li CJ (2012). Distribution and seasonal dynamics of ergot alkaloids in Elymus dahuricus- endophytic fungi symbiont.Acta Prataculturae Sinica, 21(3), 84-92. (in Chinese with English abstract)
[徐瑞, 南志标, 周雁飞, 李春杰 (2012). 披碱草内生真菌共生体中麦角生物碱的组织分布与季节动态. 草业学报, 21(3), 84-92.]
[126] Yang S, Li CJ, Chai Q, Huang X, Nan ZB (2010). Allelopathic effects of Neotyphodium endophytes of Elymus dahuricus on seeds and seedlings of three turf grass species.Acta Prataculturae Sinica, 19(4), 33-40. (in Chinese with English abstract)
[杨松, 李春杰, 柴青, 黄玺, 南志标 (2010). 披碱草内生真菌对三种草坪草种子和种苗的化感效应. 草业学报, 19(4), 33-40.]
[127] Yue Q, Miller CJ, White JF Jr, Richardson MD (2000). Isolation and characterization of fungal inhibitors from Epichloë festucae.Journal of Agricultural and Food Chemistry, 48, 4687-4692.
[128] Zhang XX, Li CJ, Nan ZB, Matthew C (2011). Neotyphodium endophyte increases Achnatherum inebrians (drunken horse grass) resistance to herbivores and seed predators.Weed Research, 52, 70-78.
[129] Zhou Y, Zheng LY, Zhu MJ, Li X, Ren AZ, Gao YB (2014). Effects of fungal endophyte infection on soil properties and microbial communities in the host grass habitat. Chinese Journal of Plant Ecology, 38, 54-61. (in Chinese with English abstract)
[周勇, 郑璐雨, 朱敏杰, 李夏,任安芝,高玉葆 (2014). 内生真菌感染对禾草宿主生境土壤特性和微生物群落的影响. 植物生态学报, 38, 54-61.]
No related articles found!
Full text



[1] Yang Ying-gen;Zhang Li-jun and Li yu. Studies on the Postharvest Physiology properties of Peach Fruits[J]. Chin Bull Bot, 1995, 12(04): 47 -49 .
[2] Zhou Shi-gong. Applications of Lanthanum in Botanical Research[J]. Chin Bull Bot, 1992, 9(02): 26 -29 .
[3] . [J]. Chin Bull Bot, 1996, 13(专辑): 105 .
[4] 杜维广 王彬如 谭克辉 郝迺斌. An Approach to the Breeding of Soybean with High Photosynthetic Efficiency[J]. Chin Bull Bot, 1984, 2(23): 7 -11 .
[5] ZHAO Yun-Yun ZHOU Xiao-Mei YANG Cai. Production of Hybrid F1 Between Avena magna and Avena nuda and It''s Identification[J]. Chin Bull Bot, 2003, 20(03): 302 -306 .
[6] . Professor Jiayang Li, a Plant Molecular Genetist[J]. Chin Bull Bot, 2003, 20(03): 370 -372 .
[7] . [J]. Chin Bull Bot, 1996, 13(专辑): 100 -101 .
[8] Qiong Jiang, Youning Wang, Lixiang Wang, Zhengxi Sun, Xia Li. Validation of Reference Genes for Quantitative RT-PCR Analysis in Soybean Root Tissue under Salt Stress[J]. Chin Bull Bot, 2015, 50(6): 754 -764 .
[9] MA Ke-Ming. Advances of the Study on Species Abundance Pattern[J]. Chin J Plan Ecolo, 2003, 27(3): 412 -426 .